The IUCN/SSC Canid Specialist Group's
African Wild Dog Status Survey and Action Plan
(1997)
Rosie Woodroffe
Many of the data compiled in this Action Plan have been collected from radio-collared wild dogs. However, it has been suggested that immobilizing wild dogs to fit radio-collars may lead to high mortality. Likewise rabies vaccination, one of a suite of measures considered for rabies control, has been blamed for wild dog deaths. The handling-immunosuppression hypothesis proposes that handling - defined as immobilization, radio-collaring and/or rabies vaccination - killed wild dogs in the Serengeti-Mara ecosystem by compromising their immune response to rabies virus. In the light of this hypothesis, it is important to assess the risks associated with handling before making recommendations for future wild dog management and research. In this Appendix, I review the available evidence and conclude that:
A scenario in which vaccination failed to protect wild dogs from exposure to rabies in the Serengeti-Mara ecosystem is much more plausible, therefore, than one which hypothesizes a causal link between handling and mortality. Since radio-collaring plays an important rôle in wild dog research, I conclude that the benefits of immobilization outweigh the risks, provided:
The rabies vaccination protocols used so far on free-ranging wild dogs seem to confer few benefits. Further research, on captive animals, is needed to establish more effective protocols. However, only rarely will direct vaccination of wild dogs represent the most appropriate strategy for disease control.
Much of the information collated in this Action Plan derives from research carried out on wild dogs in the field. Almost all intensive ecological studies of wild dogs have fitted some animals with radio-collars: these are crucial for locating packs that range very widely, often in fairly thick bush. Radio-collaring involves immobilizing animals with anaesthetic darts; this also allow the collection of samples for disease screening, genetic profiling and hormone analysis. Over the past 10 years, immobilizing wild dogs has formed a central part of research aimed at their conservation.
Two projects have administered rabies vaccines to free-ranging wild dogs. In the Masai Mara-Loita area, in Kenya, wild dogs that had been immobilized for radio-collaring were routinely vaccinated in 1988 and 1989, since rabies was known to occur in the local domestic dog population (P. Kat pers. comm.). This project also vaccinated some wild dogs without immobilizing them, delivering the vaccine by dart (P.Kat pers. comm.). In the Serengeti National Park, Tanzania, contiguous with the Masai Mara, wild dogs from two packs were vaccinated in 1990, after rabies had killed one Serengeti and one Mara pack in the previous 13 months (Gascoyne et al. 1993a; Gascoyne et al. 1993b). Vaccine was delivered by dart to 30 wild dogs, and by hand to four immobilized animals (Gascoyne et al. 1993a).
These vaccination programmes failed in their attempt to protect the wild dog population in the Serengeti-Mara ecosystem: all of the study animals eventually disappeared and today there are no wild dog packs known to be resident in either the Serengeti or the Mara study sites. Disease was implicated in the deaths of three study packs in the Mara and one in Serengeti following vaccination, and at least one of the animals vaccinated in the Mara area definitely died from rabies (L.Munson pers. comm., P.Kat pers. comm., Alexander & Appel 1994).
Following the disappearance of the Serengeti-Mara study packs, it was suggested that handling - defined as immobilization, radio-collaring and/or rabies vaccination - might be extremely harmful to wild dogs. A handling-immunosuppression hypothesis proposed that handling, perhaps in combination with some form of social stress, compromised wild dogs' immune systems leading to the reactivation of latent rabies infections (Burrows 1992; Burrows et al. 1994). Burrows and his co-authors argued that such reactivation would be followed by transmission of the virus to pack members that had not been handled, leading to rapid death of the whole pack.
This handling-immunosuppression hypothesis provoked a spirited debate in both the academic and popular press, which sometimes ranged beyond the scope of the data available (reviewed and discussed by Heinsohn 1992; Gates 1993; Morell 1995; Harper 1995; Dye 1996). If correct, the hypothesis has extremely serious implications, not only for wild dog research and conservation, but also for research carried out on other wild animals.
In this context, it is not my aim to consider all of the various arguments brought forward to explain the disappearance of wild dogs from the Serengeti-Mara study sites. However, it is the aim of this Action Plan to develop recommendations for the conservation and management of free-ranging wild dogs. It is important, therefore, to consider the risks associated with immobilization and vaccination, and to determine whether these risks might outweigh the benefits of such handling. For this reason, in this Appendix I discuss the handling-immunosuppression hypothesis, and use this discussion to evaluate the future rôle of immobilization and vaccination in wild dog management and research.
Although there were separate research projects established around the Masai Mara National Reserve (in Kenya), and in Serengeti National Park (in Tanzania), the Serengeti ecosystem spans the international border and the wild dogs inhabiting the area formed a single contiguous population (Burrows 1995). Individuals first identified in Tanzania dispersed into Kenya and formed packs with Kenyan wild dogs, and vice versa (P.Kat pers. comm., Burrows 1995; Fuller et al. 1992b), and wild dogs sampled by the two studies shared a unique mitochondrial haplotype (Chapter 2).
Rabies was confirmed in wildlife in the Serengeti ecosystem for the first time in 1986, in bat-eared foxes (Otocyon megalotis) in Serengeti National Park (Maas 1993). In the same year, all the wild dogs in one of the Serengeti study packs, the Pedallers pack, died of disease (TableA1.1; J.H.Fanshawe pers. comm.). One carcass was recovered but necropsy was inconclusive; rabies was suspected but not confirmed. One pack member had been blood-sampled prior to death and found to be seronegative for canine distemper (J.H.Fanshawe pers. comm.).
The first confirmed case of rabies in the Serengeti-Mara wild dog population was recorded in August-September 1989, when 21 of 23 members of the Aitong pack, north of the Masai Mara, died within a six-week period (Kat et al. 1995). Two of the animals that died had been vaccinated against rabies in June-July 1989 using Imrab (Rhône-Merieux), an inactivated rabies vaccine (P.Kat pers. comm., Kat et al. 1995). Despite this, necropsy of the carcasses of four pack members revealed that all were rabies-positive (Kat et al. 1995), and one of the rabies-positive carcasses was that of a vaccinated animal (L.Munson pers. comm.). Viruses were extracted from three of these carcasses, and molecular genetic analysis showed that the rabies viral variant was one common in sympatric domestic dogs (Kat et al. 1995).
In August 1990, most members of the Mountain pack, a Serengeti study pack, disappeared. One animal was found still alive, showing symptoms suggestive of rabies, and rabies was confirmed in the carcass of another pack member found dead nearby (Gascoyne et al. 1993b). As in the Aitong pack, the virus isolated from this carcass was found to be a viral variant common in local domestic dogs (Kat et al. 1995).
In 1990, Tanzania National Parks decided to implement a rabies vaccination programme in Serengeti. In September 1990 an inactivated vaccine (Madivak, Hoescht) was administered to members of the two remaining study packs, the Salei pack and the Ndoha pack (TableA1.1, Gascoyne et al. 1993a; Gascoyne et al. 1993b).
Subsequent to the confirmation of rabies in wild dogs in the Serengeti-Mara ecosystem, all of the study packs disappeared - their histories are summarized in TableA1.1. The Ndoha pack was last sighted in January 1991, then disappeared (Gascoyne et al. 1993a). The Salei pack split in late 1990, and three new packs were formed: the New Barafu, Trail Blazers and M&S packs. All of these packs had disappeared by July 1991 (Gascoyne et al. 1993a). The Trail Blazers pack was last sighted in May 1991, when two animals had disappeared and other pack members appeared lethargic; the radio-collars were found subsequently, but there were no signs of carcasses (Gascoyne et al. 1993a). A photograph showing members of the Salei pack was passed to Frankfurt Zoological Society by a tour driver, but the date on which it was taken could not be confirmed and, despite extensive searching, the tourist who took the photograph could not be traced (S.Cleaveland* pers. comm. *=formerly S. Gascoyne). The radio-collar of a member of the Salei pack was retrieved by July 1991, but the carcass was not recovered. Thus, there were no confirmed sightings of any of the Serengeti study animals after June 1991 (Gascoyne et al. 1993a).
Another pack which was not part of the Serengeti study population, the Moru Track pack, was identified in 1990 and may also have disappeared in 1991 (TableA1.1, Burrows 1995).
By 1990, only two wild dog study packs remained in the Mara study site (TableA1.1). Members of one, the Intrepids pack, were seen dead and dying in December 1990 (Alexander & Appel 1994), although eleven members of this pack had been vaccinated against rabies during the previous 13 months (P.Kat pers. comm.). A radio-collar was recovered, but no carcasses were found and the pack was not sighted again (Alexander & Appel 1994). The other study pack, the Ole Sere pack, contained a radio-collared male which had been vaccinated as a member of the Intrepids pack in January 1990 (P.Kat pers. comm.). This animal was found dead in early January 1991, and tested positive for rabies, although the sample was badly decomposed and the rabies diagnosis was not confirmed by a second laboratory (P.Kat pers. comm., Alexander & Appel 1994).
Two unmonitored packs may also have disappeared from the Mara area in 1991 (Kat et al. 1995). These packs, the Bardamat and Maji Moto packs, were seen repeatedly by farmers and missionaries to the North of the Mara study site, although they were never photographed (P. Kat pers. comm.). They were last sighted in April-May 1991, and no further sightings were reported in 1992 (P. Kat pers. comm.).
| Table A1.1 The fates of individually identified wild dog packs in the Serengeti-Mara ecosystem post-1986. Sources: (a) J.Fanshawe pers. comm.; (b) Lelo (1990); (c) Kat et al. (1995); (d) Fuller & Kat (1990); (e) P.Kat pers. comm.;(f) L.Munson pers. comm.; (g) Burrows (1993); (h) Gascoyne et al. (1993a); (i) Gascoyne et al. (1993b);(j) Alexander & Appel (1994); (k) Scott (1992) (cited by R.Burrows 1994);(l) Burrows (1994); (m) Burrows et al. (1994). | |||||
| Pack | Last seen alive | Immobilized? | Vaccinated? | Comments | Fate |
| Pedallers | June 1986 (a) | Yes; collar fitted March 1986 (a) |
No | Four dogs found dying in June 1986. Rabies was suspected although no conclusivediagnosis could be made from the one carcass that was examined. (a) | Died |
| Naabi | September 1988 (b) | Yes; last collar fitted May 1988 (b) | No | An empty radio-collar and jawbone were recovered, the rest of the pack disappeared. (b) | Disappeared |
| Aitong | September 1989 (c) | Yes; last collar fitted July 1989 (d) | Yes; three vaccinated in July 1989 (c,e) | 21 pack members died -- the carcassses of four were recovered and tested positive for rabies (c). One of these had been vaccinated (f) | Died |
| Ndutu | November 1989 (g) | Yes: last collar fitted July 1989 (h) | No | Two collars were found. Rabies was suspected but not confirmed. | Probably died |
| Lemuta | February 1990 (g) | Yes; collared February 1990 (g) | No | Seen only once, at collaring. (g) | Disappeared |
| Mountain | August 1990 (i) | Yes; last collar fitted June 1990 (i) | No | The last pack members seen aliveshowed rabies signs: one carcass was recovered which was positive for rabies, and one radio-collar was recovered in August 1990. (g) | Probably died |
| Intrepids | December 1990 (i) | Yes: last collar fitted September 1990 (e) | Yes: 11 vaccinated, last in 1990 (e) | Pack member were seen dead and dying but no caracasses were recovered (i) | Died |
| Ole Sere | January 1991 (j) | Yes; last collar fitted February 1990 (e) | Yes; one vaccinated in the Intrepids in December 1989 (e) | The carcass of the vaccinated pack member was recovered. This was found positive for rabies with one test, but negative by another. (j) | Probably died |
| Triangle (=Border Rovers) | January 1991 (k) | Yes; last collar fitted January 1991 (g) | No | Two radio-collared animals were lost in late 1990. Others were seen subsequently. | Unknown |
| Ndoha | January 1991 (h) | Yes; last collar fitted January 1991 (g) | Yes; 13 vaccinated September 1990 (h,j) | One radio-collar was retrieved in July 1991 (i) | Probably died |
| Salei | May 1991 (g) | Yes; last collar fitted February 1991 (g) | Yes, 21 vaccinated September (h,j) | One radio-collar was found but the carcass was not recovered. (h) | Probably died |
| Trail Blasers | May 1991 (i) | Yes; last immobilized November 1990 (g) | Yes; vaccinated in the Salei & Ndoha packs in September 1990 (i) | Formed in February 1991 by dispersing members of the Salei and Ndoha packs. The last pack member seen alive appeared lethargic. The two radio-collars were found in Junly 1991, but there was no sign of the carcasses (i) | Probably died |
| M & S | June 1991 (g) | Yes; last immobilized September 1990 (g) | Yes; vaccinated in the Salei pack in September 1990 (i) | Formed by breakwawy of a subodrinate pair from the Salei pack (i). Neither was radio-collared at the time of their disappearance. | Disappeared |
| New Barafu | May 1991 (g) | Yes, last collar fitted September 1990 (g) | Yes; vaccinated in the Salei pack in September 1990 (i) | Formed by dispersal from the Salei pack (h). Two collars were never recovered | Disappeared |
| Moru Track | December 1991 (m) | No | No(i) | A possibly non-resident, non-study pack first verified in December 1990 (m) | Disappeared |
Analysing data from the Serengeti study population, Burrows et al. (1994) found that whole packs and adult individuals both showed decreased longevity in 1985-1991, when routine handling occurred, compared with 1970-77 when little handling took place. Within the 1985-1991 study period, the proportion of adults and yearlings that survived for 12 months after handling was significantly smaller than the proportion of unhandled adults and yearlings that survived for 12 months after the first sighting as an adult or yearling. Animals which were vaccinated by dart survived for shorter periods than did those which were only radio-collared (Burrows et al. 1994); this association persisted when non-significant effects of age and sex were excluded from the model (Burrows et al. 1995; Ginsberg et al. 1995b), and when a later, unconfirmed sighting of the handled New Barafu pack was included (Burrows et al. 1994). Animals radio-collared after they had joined a new pack survived for shorter periods than did those collared prior to dispersal (Burrows et al. 1994).
A similar analysis of data from the Mara study population, along with four other wild dog populations, was carried out by Ginsberg et al. (1995a). This analysis found no association between handling and survivorship. However, the analysis was incomplete since it did not take into account the fact that some of the wild dogs from the Mara which were classified as 'unhandled' had, in fact, been vaccinated by dart (East 1996; Ginsberg 1996). Using published sources, Burrows et al. (1995) attempted to reconstruct the Mara dataset, identifying 24 handled and 44 unhandled individuals (cf 20 handled and 67 unhandled reported in Ginsberg et al. 1995). They hypothesized a 'best-case scenario', in which all dispersing animals were assumed to survive, and a 'worst-case scenario' in which dispersers were assumed to have died. Their calculations showed significantly higher mortality of handled animals under the 'best-case scenario', but no significant effect under the 'worst-case scenario'. They discounted the 'worst-case scenario' because it generated mortality rates they considered unrealistically high, when compared with mean mortality rates for the Mara population published in Fuller et al. (1992a), although the exact mortality for the period when handling occurred remains unknown.
As a result of these complications, neither Ginsberg et al. (1995a) nor Burrows et al. (1995) provides firm evidence for an association (or lack of an association) between handling and mortality in the Mara study population. I attempted to obtain the complete Mara dataset, but, regrettably, was unable to do so. Thus, the question of whether any such association exists remains unresolved.
After considering a whole suite of other ecological factors, Burrows et al. (1994; 1995) concluded that the handling-immunosuppression hypothesis was the most likely explanation for the associations between handling and longevity that they found in the Serengeti dataset, and for a similar association postulated for the Mara dataset. In the following sections I therefore discuss the questions I consider critical to the testing of the handling-immunosuppression hypothesis.
Burrows' hypothesis concerns the effect of handling-induced immunosuppression on rabies infection (Burrows 1992). However, several authors have suggested that some of the Serengeti-Mara study packs might have died from canine distemper (CDV) rather than rabies.
The exact reasons for the loss of study packs are often lacking - in some cases it is not even certain that pack members died (Table A1.1). No live wild dogs in either study site were ever found to be seropositive for CDV (Chapter 4). Carcasses were available from only four packs that disappeared from the Serengeti-Mara region in 1986-91 (Table A1.1). Carcasses from 3 packs were tested for rabies, and all were found to be positive (although one diagnosis was not confirmed, see above). Tissue samples from the Aitong carcasses were also tested for CDV by immunohistochemistry and found to be negative (L. Munson pers. comm.). Thus, there is no direct evidence that canine distemper played any rôle in the disappearance of wild dogs from the Serengeti-Mara study sites.
Macdonald et al. (1992) considered death from CDV a plausible explanation for whole-pack deaths, because they thought it unlikely that rabies would have killed wild dogs which had been rabies-vaccinated. Alexander & Appel (1994) reported a CDV epidemic among domestic dogs in the Mara study site in late 1990/early 1991. Thus, there is circumstantial evidence that wild dogs might have contacted CDV around the time that they disappeared from the two study sites. The next two sections therefore address questions critical to testing the hypothesis that CDV might have played a rôle in the pack disappearances.
The mortality caused by CDV in wild dogs is poorly known. The only documented outbreak involved a pack in Botswana: all pups and four of six adults died, while the remaining adults disappeared (Alexander et al. 1996). The carcass of one of the pups was recovered, and CDV infection was confirmed by immunohistochemistry; tests for rabies and parvovirus proved negative (Alexander et al. 1996). Thus, in this case CDV appears to have caused mortality on a scale similar to that which occurred in the Serengeti-Mara.
Data from elsewhere indicate that a fairly high proportion of wild dogs may survive contact with CDV: populations may show seroprevalences of 50-100% while remaining stable (Chapter 4). However, none of 28 wild dogs sampled in the Serengeti-Mara was seropositive for CDV (Chapter 4), suggesting that the population may have been naïve to CDV prior to the epidemic postulated for 1990-1. Under such circumstances high mortality would be expected. Thus, the mortality caused by CDV in wild dogs may be lower than that caused by rabies in some populations, but CDV could have caused very high mortality in the apparently naïve Serengeti-Mara population.
At least 48 of the wild dogs that disappeared from the Serengeti-Mara study sites in 1989-91 had been given inactivated rabies vaccines to protect them against rabies (Table A1.1). The vaccines used (Madivak (Hoescht), Rabisin (Rhône-Merieux) and Imrab (Rhône-Merieux), Gascoyne et al. 1993b; Kat et al. 1995; Macdonald et al. 1992) are licensed in Europe to protect domestic dogs from rabies for up to 3 years (Rhône-Merieux, pers. comm., Gascoyne 1992). Death of all of the vaccinated wild dogs, from rabies, within 13 months of vaccination would therefore be unexpected. Several explanations have been put forward, some more convincing than others:
It is possible that the vaccination protocols used did not induce protective antibody levels in the wild dogs that were treated. Most commercial inactivated rabies vaccines are licensed to give protection after a single inoculation (Rhône-Merieux pers. comm.; Intervet, pers. comm.), but this protocol may not always generate a protective antibody response. Administration of a single dose of the inactivated rabies vaccine Dohyrab (Solvay Duphar) to captive wild dogs held in the Mkomazi Game Reserve failed to generate protective antibody levels (Visee 1996). Five of 12 animals sampled before and after vaccination showed no rise in antibody titre after 10 weeks. Of the 25 that were vaccinated in total, 12 had no detectable rabies antibodies 10 weeks later, and none developed nominally protective antibody levels (rabies serum neutralizing antibody (RSNA) levels >0.5 International Units/ml are considered likely to be specific and nominally protective). Unpublished studies of captive wild dogs in South Africa suggest that animals must be given more than one dose of inactivated vaccine to establish antibody levels likely to be protective (G.R. Thomson, pers. comm). Some studies of domestic dogs show a similar pattern: for example, in Alaska domestic dogs given several doses of vaccine had higher antibody titres than did those vaccinated just once (Sage et al. 1993).
Likewise, the available evidence suggests that the single vaccination given to wild dogs in the Serengeti and the Masai Mara might have failed to generate protective antibody levels. One animal that had been vaccinated as a pup in the Intrepids pack in December 1989-January 1990 was found to be seronegative for rabies when he was immobilized for radio-collaring in September 1990 (P.Kat pers. comm.). Two animals that were blood-sampled before and after vaccination in Serengeti showed rises in antibody titres within 28 days (Gascoyne et al. 1993a). However, one was considered seropositive before vaccination (RSNA 0.55IU/ml), and the other, which was vaccinated by dart, seroconverted but developed a low antibody titre only just above that considered likely to be protective (0.55IU/ml, Gascoyne et al. 1993a). Thus there is no strong evidence that wild dogs vaccinated in the field seroconverted to high antibody titres. It is possible, therefore, that at least some of wild dogs vaccinated in the Serengeti-Mara failed to achieve protective antibody levels.
It is also conceivable that antibodies might not have remained at protective levels: 26 domestic dogs given a single dose of an inactivated vaccine licensed to provide protection for 3 years all had nominally protective RSNA levels 30 days post-vaccination, but in 7 (27%) antibody titres had fallen to <0.5 IU/ml after 60 days (Sage et al. 1993).
Taken together, these findings raise the possibility that the single dose of vaccine given to wild dogs in the Serengeti-Mara might have been insufficient to establish and maintain protective antibody levels. This would be especially likely if animals vaccinated by dart did not receive the full dose of vaccine (Burrows 1994). Animals without protective antibody levels would have been vulnerable to infection had they contacted rabies some months later.
It is conceivable, but unlikely, that the rabies strain which affected the wild dogs in the Serengeti-Mara was so pathogenic that it overcame the immunity induced by vaccination (Macdonald et al. 1992). This does seem to have occurred in the past in domestic dogs: eleven of 26 dogs which died of rabies in Gabon had been vaccinated - some of them repeatedly, using inactivated vaccines including Rabisin (Bourhy et al. 1988). Bourhy et al. (1988) commented that some African rabies strains are more pathogenic than the European strains usually used to test vaccine efficacy. However, the virus isolated from wild dog carcasses retrieved from the Serengeti-Mara was from a strain common in the local domestic dog population (Kat et al. 1995). Thus it seems unlikely that a highly pathogenic rabies strain was responsible for the disappearance of wild dogs from the Serengeti-Mara.
It is extremely unlikely that inappropriate storage of the vaccines used can explain the apparent vaccine failures. Inactivated vaccines require refrigeration, but it is known that the vaccines used in both the Serengeti and the Mara wild dog vaccination programmes were kept cool at all times (S.Cleaveland pers. comm.; P.Kat pers. comm.). Furthermore, trials carried out with Rabisin have shown that it still protects domestic dogs against rabies challenge when it has been stored for a week at 37°C before administration (Chappuis 1995).
Interference between the vaccine and maternally-derived antibodies in young animals cannot account for the putative vaccine failures, because most of the animals vaccinated were adults and yearlings (Macdonald et al. 1992).
It is impossible that the vaccine itself caused clinical rabies. Modified live vaccines may have this effect, but only inactivated vaccines were used in the Serengeti-Mara (Gascoyne et al. 1993b; Kat et al. 1995; Macdonald et al. 1992). Inactivated vaccine preparations contain only dead virus and cannot be pathogenic (Bunn 1991).
In evaluating the possibility of rabies vaccine failure in the Serengeti-Mara study populations, it is important to bear in mind that, whatever the mechanism involved, there is firm evidence that wild dogs vaccinated against rabies have died of rabies in the past. Two of three wild dogs vaccinated in the Aitong pack died during a disease outbreak in 1989: the carcass of one was recovered, and rabies infection was confirmed from tissue samples (L.Munson, pers. comm., Kat et al. 1995). Furthermore, four wild dogs released in the Etosha National Park, Namibia, died from rabies even though they had been vaccinated annually with Rabisin while held in captivity (L.Scheepers, pers. comm., Scheepers & Venzke 1995). Unexplained vaccine failures have also occurred in domestic dogs living under field conditions: 14/176 rabies cases in Texas and 13/247 cases in Mexico involved vaccinated dogs (Clark et al. 1981; Eng et al. 1994).
On the basis of these data, I conclude that it is entirely possible that rabies was responsible for the disappearance of the last study packs in the Serengeti-Mara area. Attempts to protect them from rabies by vaccination could have failed. Since there is no direct evidence to suggest that CDV killed any of the study animals, rabies remains the most likely cause of their disappearance.
Burrows et al. (1994; 1995) suggested that unhandled non-study packs persisted while packs handled by researchers disappeared in 1990-1. They calculated that the number of unknown wild dogs entering the Serengeti study area was no lower after the last study packs disappeared in 1991 than in 1985-1991. This, they claimed, showed that the population of wild dogs outside the study area had persisted (and still persists) even though all of the study packs had disappeared. Other authors have, however, contested this claim (Dye 1996; Gascoyne & Laurenson 1994).
It is difficult to keep track of wild dogs that are not radio-collared (which is the reason researchers use radio-collars to mark study packs). This means that the data on the non-study packs in the Serengeti-Mara ecosystem are extremely poor. One pack - the Moru Track pack - was identified in Serengeti from photographs taken by tourists, although it was never located by researchers (Gascoyne & Laurenson 1994). This pack was seen repeatedly in December 1990, and last sighted in December 1991 (Burrows et al. 1994). However, it is not clear whether this pack was ever really resident in the study area.
Two non-study packs, the Bardamat and Maji Moto packs, apparently disappeared from the area of the Mara study site in 1991 (see above). However, these packs were never seen by researchers, and never photographed, so sightings remain unconfirmed.
Another non-study pack, of 12 animals, was sighted from the air in the Loliondo area, to the east of Serengeti National Park, in November 1990 (S.Cleaveland pers. comm.). A pack was sighted again in this area in early 1992 but, although this group was photographed, no animals could be recognized from earlier photographs (Burrows 1993). Thus, it is not known whether a pack had persisted in the Loliondo area while those inside Serengeti study area disappeared, or whether the dogs sighted in 1992 were new arrivals. A den was reported from the Loliondo area in 1993, indicating that a resident pack was using the area at that time (S.Cleaveland pers. comm.).
All of the wild dogs sighted in the Serengeti study site since 1991 have been single-sex groups (Burrows et al. 1994). It is difficult to interpret such sightings. Dispersing groups of wild dogs may move over very large areas, and the wild dogs sighted in the Serengeti study site since 1991 may not have came from immediately adjoining areas. The distribution data presented in Chapter 3 indicate that dispersing groups of wild dogs occasionally turn up in countries where they have been locally extirpated, travelling hundreds of kilometres.
I conclude, then, that the available data are not sufficient to substantiate claims that unhandled packs definitely survived when handled packs disappeared (Burrows 1992; Burrows et al. 1994; East & Hofer 1996). Disappearance of wild dogs from the Serengeti-Mara ecosystem might not have been confined to the handled study packs. The Moru Track, Bardamat and Maji Moto packs, which were never handled, may have disappeared around the same time as the study packs. At least one pack used the Loliondo area after the study packs had disappeared. The possibility remains that this pack survived the disease outbreak when study packs died. However, even if this pack persisted through the outbreak, it is impossible to assess whether this was because it was outside the area where wild dogs were handled.
Burrows (1992) argued that handling by researchers reactivated quiescent rabies infections in the Serengeti-Mara wild dogs. Such reactivation would, he suggested, be followed by signs of disease and transmission of the virus to pack members that had not been handled. How likely is it, then, that the wild dogs that were handled were harbouring quiescent rabies infections?
Rabies is not always fatal in domestic dogs - the alternative host responses are illustrated in FigureA1.1. When a domestic dog is infected with rabies, the virus may remain latent close to the site where it entered the host, producing neither disease nor an immune response (Fekadu 1991b). Alternatively, the rabies virus may be resisted by the dog's immune system, so that the infection is aborted without the animal ever showing signs of disease. However, once the virus enters the central nervous system, symptoms of rabies begin (Fishbein & Robinson 1993). Even now, infection may not prove fatal: some domestic dogs may recover without clinical support, and a very small number have continued to excrete the virus in their saliva after recovery (FigureA1.1, Fekadu 1991b).
Data collected in Serengeti raise the possibility that rabies might not always be fatal in wild dogs. Gascoyne et al. (1993b) sampled 12 animals from five packs between 1987 and 1990, and found that three of them, from two packs, had positive titres of rabies neutralizing antibodies (5 seropositive animals were initially reported, but this was due to inconsistencies in the calculations of RSNA titres between laboratories, Burrows 1994; Gascoyne & Laurenson 1994). None of 18 wild dogs sampled in the Mara study site was seropositive for rabies (Alexander et al. 1993). The results from Serengeti must be interpreted with caution (Gascoyne et al. 1993a). It is possible that they represent a non-specific reaction: the assay used was developed for humans and had not been validated for wild dogs (S.Cleaveland* pers. comm.). Domestic dogs may have significant amounts of nonspecific virus-neutralizing antibodies in their sera, which generate low measured RSNA titres (Fekadu 1991b).
Despite these caveats, it is possible that Gascoyne et al.'s (1993b) data show that wild dogs from two packs in the Serengeti population had survived contact with rabies in the past. If this were the case, it would have two implications for the handling-immunosuppression hypothesis. First, it raises the possibility that the seropositive wild dogs might have been rabies carriers. Second, it suggests that even seronegative pack members might have had some contact with rabies and might, therefore, be harbouring latent infection. I shall discuss these two possibilities in order.
If Gascoyne et al. (1993b) detected rabies-specific serum antibodies, their results would suggest that the seropositive wild dogs had either aborted rabies infection, or contracted the disease and then recovered (FigureA1.1). It is impossible to be sure which of these alternatives is the most likely. Recovery from rabies can only be distinguished from aborted infection by looking for antibodies in the cerebro-spinal fluid (Fekadu 1991b). Cerebro-spinal fluid was not sampled in wild dogs immobilized in Serengeti for obvious ethical reasons. However, experimental studies of domestic dogs indicate that aborted infection is more common than recovery: of 28 dogs given intramuscular inoculations of a (rather avirulent) strain of rabies virus, 7(25%) aborted infection and 2(7%) recovered; the remaining dogs all died (Fekadu & Shaddock 1984; Fekadu et al. 1981).
If the seropositive wild dogs had aborted rabies infection, then handling could not have reactivated the infection, since animals which have aborted rabies no longer carry the virus. Indeed, domestic dogs that have aborted infection subsequently resist challenge with rabies virus (Fekadu & Shaddock 1984). Under this scenario, then, seropositive wild dogs might have had a better chance of surviving subsequent contact with rabies than those which had never been previously exposed. All three seropositive dogs were alive five months after sampling, and one is known to have survived 30 months (Gascoyne et al. 1993a).
If, rather than having aborted a rabies infection, the seropositive wild dogs had recovered from clinical rabies, then there is a very small possibility that they might have still been carrying the rabies virus. A few domestic dogs have recovered from rabies but continued to excrete the virus in their saliva (Fekadu 1972; Fekadu et al. 1981). However, such cases are extremely rare. From a total of 1,083 healthy unvaccinated dogs sampled in Ethiopia just five (0.46%) were rabies carriers (Fekadu 1972). Furthermore, surveys of 791 stray dogs in Buenos Aires, Bangkok, and Cairo failed to find any animals that were carrying rabies, even though rabies was endemic in all three areas (Bell et al. 1971; Botros et al. 1979; Ratanarapee et al. 1982). In the laboratory, the carrier state has been produced only once (Fekadu et al. 1981), despite the many domestic dogs experimentally inoculated with rabies virus. In experimental studies one of 28 dogs (3.6%) inoculated with an Ethiopian rabies strain subsequently became a carrier (Fekadu & Shaddock 1984; Fekadu et al. 1981). Other experiments using different, more virulent rabies strains, have demonstrated recovery but have never produced rabies carriers (Arko et al. 1973; Fekadu et al. 1982). These studies of domestic dogs suggest that it is extremely unlikely that the wild dogs found to be seropositive in Serengeti were carrying the rabies virus.
If Gascoyne et al. (1993a) detected rabies-specific antibodies in Serengeti wild dogs, this would indicate that they had been exposed to rabies virus in the past. This raises the possibility that others in the population might have exhibited another form of non-fatal rabies: latent infection. In such cases, the virus remains at or near the site of infection without provoking a humoral immune response. As a result, latent infection is extremely difficult to detect: diagnosis can only be made when the virus reactivates and the animal develops signs of disease. Latent infection cannot be distinguished from protracted incubation. In humans the virus has occasionally remained quiescent for as long as 6 years after infection (Smith et al. 1991). Since latent infection cannot be detected in vivo, it is extremely difficult to determine whether this is a common phenomenon in naturally infected animals. However, a two-year study of 63 domestic dogs found that incubation periods for experimentally infected animals varied from 7-125 days (Fekadu 1991a). The few survivors of this study subsequently showed resistance to challenge with rabies virus, indicating that they had experienced aborted rabies infection and were not still harbouring latent infections (Fekadu et al. 1982). Latent infection has not been shown to occur in wild dogs, but there is no reason to suppose that it might be more common in wild dogs than in domestic dogs.
Since few data are available on rabies pathology in wild dogs, it is impossible to quantify the rôle played by nonfatal infection in wild dog rabies. RSNA titres measured in Serengeti were low, and the assays might have detected non-specific virus-neutralizing antibodies rather than rabies-specific antibodies. Latent infection and the carrier state are extremely rare in domestic dog populations, and neither state has been shown to occur in wild dogs. I conclude, therefore, that it is highly unlikely that a significant proportion of the wild dogs handled in the Serengeti-Mara studies was harbouring the rabies virus.
Though highly unlikely, a small possibility remains that a few of the wild dogs in the Serengeti-Mara study populations might have been carrying rabies or supporting latent rabies infection. Could such an infection be reactivated if the animals were handled by researchers?
Burrows et al. (1994; 1995) proposed three mechanisms whereby different forms of handling might have reactivated quiescent rabies infection. First, the stress of immobilization for radio-collaring might have reactivated infection. Second, the drugs used for immobilization might have suppressed the wild dogs' immune systems, making them more sensitive to rabies. Third, the vaccines delivered might have had an immunosuppressive effect. Any of these might combine with social stress and contribute to immunosuppression (Burrows et al. 1994). I shall deal with the three mechanisms in order.
Experimental studies have suggested that rabies infection might be reactivated by chronic stress (McLean 1975; Soave 1964; Soave et al. 1961):
None of these experiments showed conclusively that stress caused reactivation of rabies infection, since none included a control group of individuals which was exposed to rabies but not to the stressor. An alternative explanation for the results is, therefore, that the animals which 'survived' rabies exposure (and thus passed into the experimental treatment groups) simply had longer incubation periods than those which died before they could be exposed to the stressor. Nevertheless, the possibility remains that chronic stress might reactivate latent rabies infection, or hasten death from rabies.
Observational studies have also proposed a relationship between chronic stress and rabies pathology - Maas (1993) suggested that lactation stress might account for the much higher rabies mortality in female bat-eared foxes than in males.
Evidence that acute (rather than chronic) stress might trigger the reactivation of latent rabies infection is scarce, although Fekadu (1991b) suggested that the stress of parturition might have reactivated rabies in a domestic dog which had been a healthy rabies carrier for 10 months.
The available data suggest that chronic stress is more likely than acute stress to play a rôle in rabies pathology. However, immobilization for radio-collaring appears not to impose chronic stress on wild dogs. Creel et al. (1996b) found that, in Selous, faecal corticosterone levels were no higher in wild dogs wearing radio-collars than in uncollared dogs. Furthermore, repeated sampling before and after collaring revealed no elevation in corticosterone levels (Creel et al. 1996b).
de Villiers et al. (1995) attempted to measure the acute stress caused by immobilizing wild dogs. They used plasma cortisol levels immediately after darting as an approximation of baseline levels, and showed a 2.2-fold increase in free-ranging wild dogs that had been anaesthetized. This increase is similar in size to that recorded for immobilized spotted hyaenas, suggesting that the acute stress associated with darting is no greater for wild dogs than for other large carnivores (de Villiers et al. 1995).
The stress imposed by immobilization could combine with natural social stressors to bring about rabies reactivation. Burrows et al. (1994) showed that wild dogs radio-collared after they had formed a new pack survived for shorter periods than did those collared before they dispersed. Subordinate pack members have lower glucocorticoid levels than do dominants (Creel et al. 1996a), but no data are available upon the stress involved in pack formation. Since dominant status seems to impose chronic stress, while immobilization involves only acute stress, it might be expected that social status alone would play a more important rôle than handling in rabies pathology.
In all of the laboratory studies which have claimed to show reactivation of rabies infection, either by acute or by chronic stress, clinical rabies and death have occurred rapidly. Assuming that the stressor triggered reactivation (rather than simply being administered to animals with longer incubation periods, see above), in most cases the incubation period was much shorter than that measured in newly-infected animals (9 days vs. 43 days in Soave et al.'s (1961) study; 15 days vs. 44 days in McLean's (1975) study; 42 days vs. 30-66 days in Soave's (1964) study). However, wild dogs immobilized in the Serengeti-Mara ecosystem did not disappear within days of immobilization. Twelve wild dogs radio-collared in Serengeti survived an average of 17 months (510 days) after collaring (Burrows et al. 1994), and six radio-collared in the Mara study site survived between 2.2 and 3.7 months (66-111 days Burrows et al. 1995). For comparison, the only available data on rabies in wild dogs suggest that the incubation period is normally 8-42 days (Kat et al. 1995). It seems unlikely, therefore, that the disappearance of these animals was caused by acute immobilization stress reactivating quiescent rabies infection.
One further piece of evidence argues against a rôle for immobilization stress in the disappearance of the Serengeti-Mara study animals. Burrows et al. (1994) found that animals which had been radio-collared in Serengeti survived significantly longer those which were vaccinated by dart (Burrows et al. 1994). Immobilization stress is believed to result from the disorientation that occurs as the anaesthetics start to take effect (de Villiers et al. 1995). If this is the case, one would expect radio-tagging to be more stressful than vaccination by dart gun, and, if anything, to lead to a more rapid death - the opposite of the association found by Burrows et al. (1994).
In conclusion, I consider it unlikely that the stress induced by immobilizing wild dogs played any rôle in the course of rabies infection. Immobilization imposes a mild acute stress, but there is little evidence to suggest that rabies infection can be reactivated by acute stress. Chronic stress might reactivate such infection, but there is no evidence that immobilization causes chronic stress in wild dogs. Furthermore, chronic stress would be likely to reactivate rabies infection on a timescale much shorter than the one observed.
Several studies have shown that general anaesthesia can suppress the immune system. Is it possible that immobilizing agents, rather than immobilization stress, compromised the Serengeti-Mara wild dogs' immune systems?
Felsburg et al. (1986) showed that anaesthetizing domestic dogs with methoxyflurane had a marked effect upon their lymphocyte function. Clinical work on humans has suggested that anaesthesia with ketamine (one of the immobilizing agents used in the Serengeti study, Gascoyne et al. 1993b) can depress the immune response to rabies infection and cause death (Fescharek et al. 1994). However, two pieces of evidence suggest that immunosuppression by immobilizing agents played no rôle in the disappearance of the Serengeti-Mara study packs.
First, Burrows et al. (1994) found that wild dogs which had been immobilized and radio-collared appeared to survive significantly longer than those which were vaccinated by dart. This would not be expected if immobilization, rather than vaccination, was involved in reactivating rabies infection.
Second, anaesthetics have only a short-term effect upon the immune system: experimental work has shown that domestic dogs regain their full immune capacity within 1-4 days of anaesthesia (Felsburg et al. 1986). In contrast, wild dogs disappeared from the Serengeti-Mara study sites several months after some of them had been immobilized (Burrows et al. 1994; Burrows et al. 1995).
The effect of rabies vaccination on immune responses to rabies infection depends upon whether vaccination is carried out before or after exposure to the virus.
It is extremely unlikely that rabies vaccination would cause death in wild dogs that were already carrying latent rabies infection or incubating the virus. Post-exposure vaccination is a routine component of clinical treatment for rabies exposure (Fishbein & Robinson 1993). As the virus incubates at or near the site of infection, there is no immediate humoral immune response, and, once the virus enters the nervous system, it is sequestered from the immune system (Fishbein & Robinson 1993). During the incubation period, however, a programme of intramuscular injections of rabies vaccine exposes the body to rabies antigens and allows it to mount a humoral immune response earlier than would naturally be the case (Fishbein & Robinson 1993). Thus, post-exposure vaccination takes advantage of rabies' relatively long incubation time and confers protection on the host. This means that, far from hastening death, vaccination of wild dogs immediately after exposure to rabies infection might make them more likely to survive the infection.
Vaccination immediately before exposure to rabies virus can cause immunosuppression. The immune system is confronted with both the vaccine and the viral infection simultaneously, which means that its ability to respond to the virus is reduced. This may result in the phenomenon of 'early death' from rabies. For example, of 17 domestic dogs that contracted rabies less than 30 days after being given inactivated rabies vaccine, 17(41%) died within 7 days of exposure (Clark et al. 1981) - a shorter incubation period than that seen in unvaccinated dogs (Fekadu 1991a).
It is possible, then, that if wild dogs had been exposed to rabies within a few weeks of vaccination, they might have died from the disease more rapidly than they would had they remained unvaccinated. This scenario is highly unlikely, however: wild dogs in Serengeti disappeared, on average, 7 months after vaccination (Burrows et al. 1994).
In conclusion, it appears unlikely that rabies vaccination would have triggered mortality from rabies on the timescale that was observed. Furthermore, several of the study packs that disappeared from Serengeti contained no members that had been vaccinated (TableA1.1).
This discussion has, so far, concluded that neither immobilization nor vaccination is likely to have killed the last members of the Serengeti-Mara wild dog study populations by reactivating rabies infection. Why, then, is there a statistical association between handling and decreased longevity among wild dogs in Serengeti (Burrows et al. 1994) and, perhaps, the Mara (Burrows et al. 1995; Ginsberg et al. 1995a)?
The most likely explanation for the disappearance of the Serengeti-Mara study populations is that they were killed by a disease, from which the rabies vaccination programme failed to protect them. Since most of the packs disappeared in 1990-1 (TableA1.1), the correlations reported by Burrows et al. (1994) can also be explained by the timing of handling relative to a disease outbreak (Ginsberg 1996). In the Serengeti study area, 18 wild dogs were radio-collared between 1985 and 1989. Only one or two dogs were collared in each pack, so the majority of study animals were not handled in any way. Four more dogs were radio-collared - and also vaccinated - in 1990. Thus, 18 of the 22 dogs (82%) were radio-collared at least a year before the pack disappearances that occurred in 1990-1.
Also in 1990, an additional 30 dogs were vaccinated by dart in Serengeti. Thus, 34 of the 52 dogs (65%) that were either radio-collared or vaccinated in 1985-90 were handled in 1990. As a result, most of the handling carried out on the study population in 1985-90 was done in 1990, immediately before the putative disease outbreak.
Most of the wild dogs that were assumed to have died in Serengeti in 1985-91 disappeared along with their whole packs (Burrows 1995). Of 11 packs studied in 1985-91, eight disappeared in 1990-1 (TableA1.1, Burrows 1995). Thus, most of the wild dogs that were presumed to have died did so in 1990-1, at the time of the putative disease outbreak. For this reason, Burrows et al. (1994) excluded the 1990 data from their calculations of mortality during the period of intensive study in 1985-91 (Burrows et al. 1995). The 1990 data were, however, necessarily used in their calculations of the longevity of immobilized and dart-vaccinated animals (Burrows et al. 1994).
Given these circumstances, it is not surprising that the data show radio-collared dogs to have survived longer than dart-vaccinated dogs in Serengeti. The majority of animals were collared in 1985-9, but all of the vaccinations were carried out in 1990. Thus, vaccinated animals had less time to live before the 1990-1 disease outbreak than did radio-collared dogs. In the same way, it is not surprising that unhandled dogs survived longer than handled dogs. The majority of handling occurred in 1990, but most of the unhandled animals were identified for the first time in 1985-9. Thus, wild dogs which had been handled survived for a shorter period before the 1990-1 disease outbreak than did unhandled wild dogs.
These results mean that the association between handling and reduced longevity in Serengeti can be explained without assuming any causal relationship. As discussed above, the question of whether a similar association occurs in the Mara data set remains unresolved; likewise, data are not available to assess whether an argument similar to that outlined above might explain the association that has been hypothesized (Burrows et al. 1995).
Having reviewed the available evidence, I conclude that:
On the basis of these findings, I conclude that the handling-immunosuppression hypothesis is not the best explanation for the disappearance of the wild dog study packs from the Serengeti-Mara ecosystem. There is no realistic mechanism by which either immobilization or vaccination could have hastened death of study packs by reactivating latent rabies infection. In contrast, rabies vaccination is known to have failed on at least two occasions. A scenario in which vaccination failed to protect wild dogs from exposure to rabies is much more plausible, therefore, than one which hypothesizes a causal link between handling and mortality.
The probability that wild dogs died in the Serengeti-Mara study populations as a direct result of immobilization is very small. Nevertheless, it can never be proven that immobilization was entirely harmless. It is important to determine, then, whether the possible risks of immobilizing wild dogs outweigh the benefits.
Additional information about the relationship between immobilization and mortality comes from other studies of wild dogs. Ginsberg et al. (1995a) analysed data from 353 wild dogs studied in four areas of East and southern Africa. Data from these populations are not directly comparable with those from the Serengeti-Mara, since none of the study populations had a known history of rabies exposure (East 1996). Nevertheless, these data do provide useful information about the general risks of immobilizing and radio-collaring wild dogs. In these four populations at least, immobilization was not associated with any reduction in wild dogs' probability of survival (Ginsberg et al. 1995a).
What, then, are the benefits of immobilization? Chapter8 of this Action Plan calls for continued research into population processes in wild dogs. The majority of wild dog researchers agree that immobilization to fit radio-collars is an essential part of their work. Locating wild dog study packs without the aid of radio-collars is extremely difficult. While the Serengeti wild dog population occupied areas of open plains habitat, most other studies (and most other wild dog populations) occupy fairly thick bush. At the start of the wild dog project in Selous, researchers took a year to radio-collar just two packs (S.R. & N.M.Creel, pers. comm.), while in Hwange it took over a year to locate and re-collar a pack in which both radio-transmitters had failed (J.R.Ginsberg pers. comm.). Once animals are collared, radio-tracking allows researchers to locate wild dog packs, and thus to collect data on wild dogs' health, causes of mortality, interactions with human activity, contacts with other carnivores, including lions, hyaenas and domestic dogs, and many other topics important to wild dog conservation.
A secondary benefit of immobilizing wild dogs for radio-collaring is that it allows researchers to collect tissue samples. Such samples include blood and tissue taken for disease screening - since disease represents such a serious threat to wild dog populations, knowledge of the diseases to which they are exposed may be crucial in formulating local management plans. Genetic samples can also be collected to study both the effects of inbreeding and the subspecific status of various wild dog populations (See Chapter 2).
I conclude, therefore, that the benefits of immobilization outweigh the risks, provided immobilization is carried out in the course of research aimed at wild dog conservation. It is vital that radio-collaring be followed by an efficient monitoring programme, to check that all handled animals remain healthy, and to ensure that the very best use is made of the opportunities offered by radio-collaring. Monitoring of animals radio-collared in Serengeti was inadequate, and this contributed to the confusion over their ultimate fate. In the light of such considerations, the IUCN/SSC Canid Specialist Group's 'Workshop on the conservation & recovery of the African wild dog', held in Arusha in 1992, resolved that:
"Research which involves intervention is only justified where the planning and execution of a project give a reasonable expectation that the rewards for wild dog conservation will outweigh the costs. To ensure this fruitful outcome project planning and execution should always involve close liaison with local governmental policy-making agencies, and extensive consultation with appropriate colleagues."
As with any endangered species, the number of wild dogs handled should be kept to a minimum, without sacrificing scientific validity. The greatest of care should be taken to minimize stress to immobilized animals. Wherever possible, alternatives to handling should be explored: for example, efforts should be made to use samples that can be collected without immobilization (e.g. faeces, Creel et al. 1996b). Finally, all animals that are immobilized should be screened for disease.
New projects planned on wild dogs may benefit from contacting the IUCN/SSC Canid Specialist Group for detailed advice on handling protocols - it has established a Lycaon Working Group, chaired by Dr. M.G.L. Mills, to assist in such cases.
It is extremely unlikely that rabies vaccination caused the deaths of any of the Serengeti-Mara study animals. Nevertheless, rabies vaccination did not prevent pack extinctions. Although administering inactivated rabies vaccines to wild dogs seems to have no detrimental effects in captivity (de Villiers et al. 1995; Gascoyne et al. 1993b; Visee 1996), the vaccination protocols used in the field may have failed to stimulate sustained protective antibody levels. So far, then, the possible risks of vaccination appear to outweigh the benefits.
As discussed in Chapter 6, direct vaccination of wild dogs will rarely represent a viable option for protecting free-ranging populations from rabies. In thick bush, and in areas where wild dogs are neither radio-collared nor individually identified, vaccination programmes would be near-impossible or, at best, extraordinarily expensive. Nevertheless, direct rabies vaccination would be an option in small well-monitored populations, such as those re-established by reintroduction. Further vaccine trials are therefore needed to devise rabies vaccination protocols more likely to provide protection in such areas - details of the questions to be addressed are given in Chapter 8. Elsewhere, wildlife managers should consider the alternative strategies for rabies control detailed in Chapter 6.
Diseases other than rabies, notably CDV, also represent threats to wild dogs (Chapter 4). However, live bCDV vaccines may induce distemper in wild dogs (Durchfeld et al. 1990; McCormick 1983; van Heerden et al. 1989), and inactivated vaccines appear ineffective (Visee 1996). Thus, the risks of vaccination against CDV clearly outweigh the benefits at present.
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