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Morbillivirus infections in wildlife (in relation to their population biology and disease control in domestic animals)
veterinary microbiology Veterinary
Microbiology
44 ( 1995) 319-332
Morbillivirus infections in wildlife (in relation to their population biology and disease control in domestic animals) E.C. Anderson Wildlife Unit, Veterinary Research Laboratory, P.O. Box CY 551, Causeway. Hat-are. Zimbabwe Accepted 4 January
1995
Abstract The three members of the morbillivirus genus that infect wildlife in ecosystems where domestic animals occur are rinderpest, peste des petits ruminants (PPR) and canine distemper. Data on the relative susceptibility of species of the Order Artiodactyla for rinderpest have been obtained from historical records of outbreaks. Rinderpest in wildlife has only occurred in equatorial and eastern Africa since the great pandemic of 1889-1897. The distributions, densities and population dynamics of susceptible species in this region are described. There has only been one recorded outbreak of PPR in wildlife but the possibility of its occurrence in the future now that it is present in many parts of west and eastern Africa is discussed. Wild camivora are not likely to be important maintenance hosts for canine distemper but the disease is of significance in free-ranging carnivores and particularly in small populations of endangered susceptible wildlife species. It is also of great significance in zoo populations. Keywords: Morbillivirus;
Wildlife; Population
biology; Disease control
1. Introduction There are three members of the morbillivirus genus that infect susceptible wildlife in ecosystems that also contain domestic animals. These are rinderpest, peste des petits ruminants (PPR) and canine distemper. The wildlife hosts for rinderpest and PPR viruses are probably similar and all belong to the Order Artiodactyla (Scott, 1964). Canine distemper virus has been reported to infect members of the families Canidae, Mustelidae, Procyonidae and Viverridae of the Order Camivora and possibly also some members of the families Protelidae, Hyaenidae and Felidae (Budd, 198 1) . The occurrence of canine distemper in terrestrial carnivores is reviewed in this issue by Appel and Summers 0378-1135/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDZO378-1135(95)00026-7
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Microbiology
UGANDA
1929 Kob Buahbuck Warthog
Fig.
1960
50x
60X
Buffalo
18uffalo
44 (1995) 319-332
Eland Kudu Warthog
Bushbuck
Bushbuck
Bongo
Giraffe
40%
1
Impala Oryx
1
1,Wildlife species affected in outbreaks of rinderpest in Africa.
( 1995). The occurrence of canine distemper in mustelids in southwest Germany and the possibility that they act as reservoirs of infection for dogs is reported in this issue by van Moll et al. ( 1995).
2. Rinderpest and PPR Apart from one reported incident (Furley et al., 1987) of PPR all the outbreaks of morbillivirus infections in wild Artiodactyla have been caused by rinderpest virus. Those that occurred up to the mid-1960s have been reviewed by Plowright ( 1982; Plowright, 1985; Plowright, 1988) and Scott ( 1981). Since that time there have been very few records of rinderpest in wildlife. It occurred in 1982 in north Tanzania and in 1983 in Nigeria. Wildlife were also reported to be affected in 1984 when the disease spread from either Chad or Sudan into the highly susceptible populations in the Central African Republic (Plowright, 1985). 2.1. Susceptibility
of wildlife species
Rinderpest Data on the susceptibility of wildlife in Africa histories of outbreaks (Fig. 1). Two factors had susceptibility of different species. These were: 1. whether the population was immunologically present. 2. the virulence of the infecting strain. In endemic situations or following infection with animals succumbed. In the great African pandemic
has been obtained from the recorded an influence on the apparent relative naive or there was endemic
disease
a mild strain, only the most susceptible of 1889-1897 all species of wildlife
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Table 1 Wildlife species recorded as having been infected with rinderpest in India Family
Genus
Common name
Bovidae
Boselaphus Eibos
Nilgai Gaur Banteng Four-homed antelope Sambhar Hog deer Barking deer
Cervidae
Tetracerus cervus Axis Muntiacus
were affected with devastating results and this was largely responsible for the present day distribution of these species in Africa. There were exceptions however, as for example in South Africa, where impala (Aepyceros melampus), hartebeest (Alcelaphus spp) and wildebeest (Connochaetes taurinus) were said to have escaped. Since that pandemic all reported occurrences of rinderpest in wildlife have been in the equatorial region of central and eastern Africa with a single incident in 1983 in Nigeria (Shathikumar et al., 1985). The species most commonly affected were buffalo (sylzcerus caffer) , eland ( Taurotragus oryx) and warthog (Phacuchuerus aethiupicus) . From this history it was possible to draw up a list of species in order of susceptibility and such a list has been published (Plowright, 1982). The incidence of rinderpest has been much reduced since the introduction of the Pan African rinderpest campaign (PARC) at the beginning of 1985. Eradication of the disease from Africa is the goal and this has already resulted in the large populations of wildlife becoming susceptible once more. There is again the potential for epidemics involving wildlife populations where even the smaller populations of the putatively less susceptible species could be significant in epidemiological terms. Should this occur there could be significant mortality in some species. Species occurring on the Indian subcontinent reported as being susceptible are given in Table 1. PPR Almost nothing is known about the occurrence of PPR in African wildlife although the virus is now present in north-east, west and east Africa. The only report has been that of Furley et al. ( 1987) who reported that Dorcas gazelle (Gazella dorcas) and gemsbok ( Oryx gazella) held in a zoological collection in the Arabian Gulf died. Nilgai (Boselaphus tragocamelus) were also subclinically affected. Presumably all the antelope species are potentially susceptible for PPR. Some species occur in very large numbers (Figs. 34) while others such as the gazelle (Gazella spp.), bushbuck (Tragelaphus scriptus), impala, and duiker ( Cephalophus spp), although not occurring in large numbers, are very widely distributed throughout the region and occur in most of the pastoral areas alongside sheep and goats. This suggests that PPR infection in antelope might become of much greater significance in the future. This could also apply to the Middle East where significant populations of some antelope species still occur in the nomadic pastoral areas.
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Microbiology 44 (199.5) 319-332
Mara Serengeti Tsavo Ngorongoro Tarangire Mikumi Rungwa Kilombero Ruaha Katavi Selous National
BUFFALO Source
AND - SWRI
Fig. 2. Distribution
Parks
and
wildlife
WILDEBEEST
Buffalo
Wildebeest
2.000 43. 546
1. 146. 000
1. 963
il. 847
23. 816 12.410 t3.393
12. 474 -
24. 197
59. 261 31. 263 93. 792 157. 536
63. 202
areas
POPULATION
DENSITIES
- EAST AFRICA
report 1988 and density of buffalo and wildebeest populations
in East Africa.
3. Population biology Of central importance for the establishment, persistence and spread of microparasites to other species is the magnitude of the basic reproductive rate (Anderson and May, 1986; Anderson, 1991). Its principal determinants are host density and birth rate. The critical host density for rinderpest is determined by the relative susceptibility of the species and the virulence of the infecting virus strain. For morbillivirus infections, which are horizontally transmitted and give rise to a lasting immunity in surviving animals, the critical host density is large. The basic reproductive rate of rinderpest virus in wildlife populations is also increased where the probability of transmission by contact is greatest i.e. in species which form herds (buffalo, wildebeest, white-eared kob (Kobus spp.) , tiang (Damdiscus spp.) and which migrate (wildebeest, white-eared kob) . The reproductive rate is decreased where the infecting strain is highly virulent or the infected species is very susceptible resulting in high mortality, when the infecting strain is mild or the species has an innate resistance and also in adverse conditions such as drought and when there is high predation or poaching and human encroachment. With these principles in mind the population biology of the most susceptible and abundant species will be considered in relation to distribution, population density and population dynamics (movement/range; behaviour, i.e. herds or solitary; and reproductive rate). 3.1. Distribution The current distribution of buffalo in East Africa is shown in Fig. 2 and those of the antelope in eastern Africa in Figs. 34. These clearly indicate the large concentrations of susceptible species that are distributed throughout this region which could, theoretically, act either as reservoirs of infection or contribute to the spread of the disease. In spite of these very large populations of wild herbivores, the disease disappeared from the wildlife populations of northern Tanzania in the early 1960s and was not sustained in
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44 (1995) 319-332
AND IOW 60.000 -36.000 10. 000 70.000 13.800 10.000 4.500
TRAGELAPHINES
GAZELLE
Fioan/Sable)
Source:
East.1998.
Fig. 3. Distribution and density of wildebeest, East Africa (data from East, 1988).
IUCN Antelope
eland, gazelle (Thomsons
survey.
and Grant), roan and sable antelope in
the wildlife there following its recurrence in buffalo in this region in the early 1980s (Anderson et al., 1990). In view of the fact that these wildlife populations are increasingly encroached upon by the expanding human populations, it seems unlikely that they would act as a reservoir of rinderpest infection in the future. However, were it to be re-introduced from cattle, they could be significant in amplifying the virus and contributing to its spread. SUDAN
u
Tiang
Uganda kob ?
#
White-eared e50.000
714.000 kob
-
Giant
eland
18. 000 common
Lelwal
hartebeast
eland
io.000 &#z
Source:
East, 19EB -1UCN
Fig. 4. Distribution and density of White-eared Sudan (data from East, 1988).
and Uganda kob, tiang, eland, lechwe and hartebeest in southern
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3.2. Population density Rinderpest can establish infection in relatively small populations of susceptible species but large populations are necessary for infection to be sustained. A classic example of this was the presence of enzootic disease between the 193Os-1964 in the large concentrations of wildlife in north Tanzania (Plowright, 1982). Highly virulent strains will theoretically require larger populations in order to persist than strains of lower pathogenicity (Rossiter and James, 1989). It is only in Africa that sufficiently large numbers of susceptible wildlife occur to be of significance in the epidemiology of rinderpest. Population densities in the Middle East and India are likely to be too small. 3.3. Movement/range The range or migratory habits of each species determines the contact rate between herds of either the same or different species and therefore has an important bearing on the transmission potential of each species. There are two examples where very large numbers of animals migrate in a seasonal pattern over a large area. These are the wildebeest population ( 1.2 million) of the Serengeti ecosystem (Figs. 2-3) and the white-eared kob ( 850 000) in the Nile region of southern Sudan (Fig. 4). Such large populations have theoretically the potential to sustain the virus and spread it to other animals. However, as already stated, rinderpest disappeared from the Serengeti wildebeest populations in 1964 (Plowright, 1982) and the disease has never been reported in the large herbivore populations of southern Sudan. The reasons for this are unclear. The other species that may range quite widely but which is not as numerous is the eland (Fig. 3). This is a very susceptible species in which infection will be able to establish itself. Populations are too small for this species to sustain infection but it could, theoretically at least, contribute to the spread of infection. 3.4. Behavioural patterns Morbillivims infections require close contact for transmission to occur and therefore transmission is more likely in species which form herds such as buffalo, wildebeest, kob and eland. The contact rate between solitary animals, such as bushbuck and duiker as well as those which only form small groups such as giraffe (Giraffa camelopardalis), topi (Damaliscus korrigum) , warthog, impala, roan (Hippotragus equinus), sable (Hippotragus niger), waterbuck (Kobus ellipsiptymnus) and kudu ( Tragelaphus spp.) is much lower. 3.5. Reproductive rate The net birth rate determines whether infection is simply established or whether it is able to persist (Anderson and May, 1986). Factors that affect this in wildlife populations include climate (drought causes significant losses in newborn animals) predators and diseases affecting reproduction (bovine viral diarrhoea, brucellosis) or causing debility (tuberculosis). In the higher rainfall belts of the rinderpest enzootic region of Africa some wildlife species give birth over an extended period while others, such as the impala, have two distinct
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44 (199.5) 319-332
37.5
k_/,--&d’ Fig. 5. Distribution
of African buffalo (from Lessard et al.. 1990)
annual breeding seasons. Buffalo calves in the Serengeti, for example, are born between December and July each year and therefore susceptible young animals are present throughout the year in this and other similar areas. Calving in wildebeest populations is more seasonal and takes place once a year but the calving period extends over several months. Such is also the case with the tiang and kob in southern Sudan and Uganda. In these situations, should the initial herd immunity, through the presence of enzootic disease, be low or should the infecting strain be of low virulence, and as the herd size is sufficient, it would theoretically be possible for such a seasonality of calving to allow the persistence of infection (Rossiter and James, 1989). The recruitment rate for any population is approximately twenty percent per year. Although predators will account for some of this there is a very significant number of young susceptibles present in an enzootic area.
4. Consideration
of the significance
of some individual
species
4.1. Buffalo (syncerus cafser) Buffalo are still widely distributed throughout equatorial Africa (Fig. 5). This distribution coincidentally is similar to the rinderpest endemic regions. The densities of different pop-
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44 (1995) 319-332
Buffalo populations in 4 regions of Serengeti Number 30,CilO
0 North
West
Southwest
From: Serengeti Wildlife Research Centra Report 1930-92
Fig. 6. Buffalo populations
in the Serengeti National Park.
ulations are only currently known with any accuracy for eastern Africa (Fig. 2). In Kenya buffalo are widely distributed occurring in Laikipia district, in the Mt Kenya and Aberdare forests, Tana river, the Tsavo Nationai Park and in the Mara National Park which forms the northern tip of the Serengeti ecosystem. The population is estimated at 17-35 000 (R. Kock, personal communication). These populations are large enough and wide enough in their distribution to allow the establishment of infection and to contribute to the dissemination of the disease but not large enough to sustain it. In Tanzania the total buffalo population numbers about 500 000 and is also widely distributed. The largest concentration occurs in the Selous Game reserve but there are significant numbers in all the other areas. Apart from the tsetse infested areas of west and south Tanzania there are also significant populations of domestic animals in all these areas. Again it is doubtful if any single population would be large enough to maintain rinderpest infection on its own. It was estimated that a population of half a million would be required for measles to persist in a human population (Black, 1975). It was in the Serengeti ecosystem of northern Tanzania and southern Kenya that rinderpest became endemic in the late 1920s and remained so until 1964. There are four distinct buffalo populations in the Serengeti National Park (Fig. 6) that occur in the north, west, central and south-west. These populations are separated by quite large distances devoid of buffalo. The range of any buffalo herd does not exceed a radius of some 50 km and in the Serengeti contact between these populations does not occur. Even between contiguous herds, contact may be transitory (Sinclair, 1977). Following the outbreak of rinderpest in buffalo in the north of the Serengeti in 1982 and deaths of buffalo and eland in the Ngorongoro conservation area, a serological survey was carried out between 1987-1989 (Anderson et al., 1990) which showed that buffalo in the Tarangire National Park had also been infected (Fig. 7). The question of how infection spread between these discrete buffalo populations remains open. In the Serengeti, was it via the vast migratory wildebeest population or
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L.
Victoria
TANZANIA
A
LOCATIONS
OF SEAO-POSITIVE
Fig. 7. Places in northern Tanzania outbreak of the disease in 1982.
BUFFALO
where buffalo positive for rinderpest
antibody
were found following
the
perhaps by the widely distributed and wide ranging eland population? Did the surrounding nomadic cattle population play a part? Unfortunately, these populations were not investigated. The disease, however, did not persist in these populations (Anderson et al., 1990) and there is no evidence that it spread to buffalo populations in southern Kenya (Rossiter, personal communication). 4.2. Wildebeest (connochaetes
taurinus)
The importance of this species, which occurs in vast numbers ( 1.2 million) in northern Tanzania and southern Kenya (Figs. 2-3), has been appreciated since the 1920s. The numbers of wildebeest in the Serengeti have risen markedly over the last 20 years (Fig. 8) increasing their potential as a reservoir of infection. There are also some 63 000 present in the Selous game reserve in the south of Tanzania. The large population in the Serengeti should theoretically be able to sustain rinderpest infection. This has not occurred (Plowright, 1982), possibly due to the innate resistance that this species has to infection. 4.3. Eland (taurotragus
oryx)
The wide distribution of eland is shown in Figs. 3-4 and they also occur in significant numbers. In Tanzania there are about 60 000 eland (Serengeti-13 813; Rukwa Ruaha5000; Tabora-1800; Tarangire-Simanjiru-10 000; Selous-5-11 000). In Kenya their numbers are estimated at 50 000-60 000. In southern Sudan there are an estimated 10 000 common eland and 18 000 giant eland (East, 1988). Eland form herds of 20 to 80 individuals. They may range over an area of up to 100 km*. They also occur in habitats frequented by domestic animals as well as in the wildlife areas of the region. The densities of individual
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Serengeti Population
44 ( 1995) 319-332
Wildebeest Population (millions1
Estimates
2
1965
1955
m Serengeti
1975
Wildlife
zebra
pl
wildebeest Research
Fig. 8. Increase in the wildebeest population
1989
19e5
YEAR Centre
Report
1988-89
of the Serengeti National Park since 1955.
populations are insufficiently large to maintain infection could contribute to the dissemination of the disease.
but, as mentioned
above, they
4.4. White-eared kob, tiang and hartebeest
All these species occur in very large numbers be able to sustain persistent infection. It is known rinderpest in 1929-193 1 (Scott, 1981) but there in the larger populations of white-eared kob, tiang
in southern Sudan (Fig. 4), sufficient to that the Uganda kob were decimated by is no record of rinderpest ever occurring and Lelwel hartebeest in southern Sudan.
4.5. Overall perceived signijicance of African artiodactyla in the epidemiology of rinderpest Combining what is known about the relative susceptibility of different species, and taking into account those aspects of their population biology discussed above, the likely significance of each wildlife species in any future outbreaks of rinderpest in Africa is shown in Table 2.
5. Canine distemper 5.1. Susceptibility of terrestrial species This subject is addressed by Appel and Summers ( 1995). Species reported to be susceptible (Budd, 198 1) are listed in Table 3. The disease was responsible for the extirpation of the black-footed ferret (Mustela nigripes) from the wild (Thome and Williams, 1988). The disease has also been reported in the black-backed jackal ( Canis mesomelas) (Moehl-
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44 (I 995) 319-332
Table 2 The perceived significance of members of the Order Artiodactyla, taking into account their relative susceptibility and their population dynamics, in the maintenance and spread of rinderpest Species
Susceptibility
Density and Distribution
Buffalo (Swrcerus caffer) Wildebeest (Connochaetes taurinus) Eland (Taurotragus oryx) Kob (Kobus kob thomasi, leucotis) Giraffe (Giraffa camelopardalis) Warthog (Phacochoerus aethiopicus)
+++ ++ +++ +++ ++ +++ ++ ++ +++ ++ ++ ++ ++ + ++ ++ ++ + + + +/-
+++ +++ ++ ++ ++ + ++ ++ + + + + + ++ + + + + + + + + +
Oryx (Oryx gazella)
Topi (Damaliscus korrigum) Kudu (Tragelaphus spp. ) Bushbuck (Tragelaphus scriptus) Reedbuck (Redunca spp. ) Sitatunga (Tragelaphus spekei) Bushpig (Potamochoerus porcus) Impala (Aepyceros melampus) Waterbuck (Kobus ellipsiprymnus) Roan (Hippotragus equinus) Sable (Hippotragus niger) Duiker (Cephalophus sp. ) Oribi (Ourebia) Steinbok (Raphicerus campestris) Hartebeest (Alcelaphus spp.) Hippopotamus (Hippopotamus amphibus) Gerunuk (Litocranius walleri)
+I+/-
man, 1983), the bat-eared fox (Otocyon megalotis), mongoose ( Viuerridae) and hyaena ( Crocuta crocuta) (Plowright, 1988), the masked palm civet (Paguma Zarvata) (Machida et al., 1992) and coyotes (Canis Iatrans) (Gese et al., 1991). In a study on the causes of mortality in grey foxes ( Urocyon cinereoargenteus) in east-central Alabama, Nicholson and Hill ( 1984) reported that 35 percent were due to distemper. Isolation of morbilliviruses has also been reported from red squirrels (Sciuris uulgaris) (Vizoso, 1968) and hedgehogs (Erinaceus europaeus) (Vizoso and Thomas, 198 1) . Table 3 Species in the order Camivora
reported to be susceptible
to canine distemper
Family
Species
Canidae Mustelidae Procyonidae Vivemidae Protelidae’ Hyaenidae * Felidae * Viverridae *
foxes, wild dog, jackal, dingo, coyote, wolf weasel, ferret, mink, badger, stoat, martin kinkajou, racoon. panda, coati civet aardwolf hyaena lion genet, mongoose
* Species possibly susceptible
to canine distemper but insufficient evidence.
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More recently there have been serious outbreaks of canine distemper in captive lion (Pa&era Zeo), tiger (P. tigris), leopard (P. par&s) and jaguar (P. onca) in California and in free-ranging lion in the Serengeti National Park in Tanzania ( Appel and Summers, 1995). The possibility that mustelids act as reservoirs of infection for dogs in Germany is discussed by van Moll et al. ( 1995). 5.2. Population
biology
Distribution and density Susceptible species are generally widely distributed. They occur singly, in pairs or in groups, as for example with the Cape hunting dog (Lycaon pictus) where groups average 8-12 individuals though they can contain up to 35 dogs. Bat-eared fox form groups of up to 15 when feeding. How the disease was introduced to the lion population of the Serengeti remains to be determined but there was sufficient contact within the lion population to allow the spread of the disease which has resulted in a high mortality rate. Range Most species have a limited range but there are exceptions as with the Cape hunting dog which ranges over an area of 1,500-4000 km* in the Kruger National Park in South Africa and over a range of 450 km* in East Africa (Skinner and Smithers, 1990). Reproductive rate This can be quite significant on an individual basis. Thus the Cape hunting dog will have 2-19 pups. However the average litter size of the bat-eared fox is four while that of the black-backed jackal is only two. This latter figure reflects more closely the reproductive rate of the group as a whole which is therefore not large.
6. Conclusions Sufficient densities of wildlife to sustain rinderpest in the enzootic regions of Africa presently exist only in eastern Africa. These wildlife populations are totally susceptible to rinderpest. If a virulent strain were again to be introduced to these populations they would, in all probability, once more be decimated. Less virulent strains would probably also result in significant losses. There is, however, no evidence to support the theory that these wildlife species would remain as reservoirs of rinderpest infection. The fact that the disease was unable to maintain itself after 1964 in the large wildlife populations of northern Tanzania following control of the disease in cattle supports this. Rinderpest has never been reported in the large wild herbivore populations of southern Sudan. There are probably insufficient numbers of susceptible wildlife species in either the near East or India to be of significance. With regard to PPR very little is known about its ecology in wildlife. It is a disease that is more difficult to detect, which causes mild infections in the very large and widely distributed populations of small domestic ruminants, and one at which no control measures
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331
are currently directed. It is possible that it will become endemic in Africa’s wildlife if it has not already done so. Canine distemper will continue to be of significance in the endangered susceptible wildlife species and in zoological collections but its occurrence in wildlife has little or no significance for its control in domestic animals.
Acknowledgements I would like to thank Dr Brian Perry and Dr Russ Kruska of the International Laboratory for Research on Animal Diseases (ILRAD), Nairobi for providing the figure on buffalo distribution in Africa.
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Morbillivirus infections in wildlife (in relation to their population biology and disease control in domestic animals) E.C. Anderson Wildlife Unit, Veterinary Research Laboratory, P.O. Box CY 551, Causeway. Hat-are. Zimbabwe Accepted 4 January
1995
Abstract The three members of the morbillivirus genus that infect wildlife in ecosystems where domestic animals occur are rinderpest, peste des petits ruminants (PPR) and canine distemper. Data on the relative susceptibility of species of the Order Artiodactyla for rinderpest have been obtained from historical records of outbreaks. Rinderpest in wildlife has only occurred in equatorial and eastern Africa since the great pandemic of 1889-1897. The distributions, densities and population dynamics of susceptible species in this region are described. There has only been one recorded outbreak of PPR in wildlife but the possibility of its occurrence in the future now that it is present in many parts of west and eastern Africa is discussed. Wild camivora are not likely to be important maintenance hosts for canine distemper but the disease is of significance in free-ranging carnivores and particularly in small populations of endangered susceptible wildlife species. It is also of great significance in zoo populations. Keywords: Morbillivirus;
Wildlife; Population
biology; Disease control
1. Introduction There are three members of the morbillivirus genus that infect susceptible wildlife in ecosystems that also contain domestic animals. These are rinderpest, peste des petits ruminants (PPR) and canine distemper. The wildlife hosts for rinderpest and PPR viruses are probably similar and all belong to the Order Artiodactyla (Scott, 1964). Canine distemper virus has been reported to infect members of the families Canidae, Mustelidae, Procyonidae and Viverridae of the Order Camivora and possibly also some members of the families Protelidae, Hyaenidae and Felidae (Budd, 198 1) . The occurrence of canine distemper in terrestrial carnivores is reviewed in this issue by Appel and Summers 0378-1135/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDZO378-1135(95)00026-7
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UGANDA
1929 Kob Buahbuck Warthog
Fig.
1960
50x
60X
Buffalo
18uffalo
44 (1995) 319-332
Eland Kudu Warthog
Bushbuck
Bushbuck
Bongo
Giraffe
40%
1
Impala Oryx
1
1,Wildlife species affected in outbreaks of rinderpest in Africa.
( 1995). The occurrence of canine distemper in mustelids in southwest Germany and the possibility that they act as reservoirs of infection for dogs is reported in this issue by van Moll et al. ( 1995).
2. Rinderpest and PPR Apart from one reported incident (Furley et al., 1987) of PPR all the outbreaks of morbillivirus infections in wild Artiodactyla have been caused by rinderpest virus. Those that occurred up to the mid-1960s have been reviewed by Plowright ( 1982; Plowright, 1985; Plowright, 1988) and Scott ( 1981). Since that time there have been very few records of rinderpest in wildlife. It occurred in 1982 in north Tanzania and in 1983 in Nigeria. Wildlife were also reported to be affected in 1984 when the disease spread from either Chad or Sudan into the highly susceptible populations in the Central African Republic (Plowright, 1985). 2.1. Susceptibility
of wildlife species
Rinderpest Data on the susceptibility of wildlife in Africa histories of outbreaks (Fig. 1). Two factors had susceptibility of different species. These were: 1. whether the population was immunologically present. 2. the virulence of the infecting strain. In endemic situations or following infection with animals succumbed. In the great African pandemic
has been obtained from the recorded an influence on the apparent relative naive or there was endemic
disease
a mild strain, only the most susceptible of 1889-1897 all species of wildlife
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321
Table 1 Wildlife species recorded as having been infected with rinderpest in India Family
Genus
Common name
Bovidae
Boselaphus Eibos
Nilgai Gaur Banteng Four-homed antelope Sambhar Hog deer Barking deer
Cervidae
Tetracerus cervus Axis Muntiacus
were affected with devastating results and this was largely responsible for the present day distribution of these species in Africa. There were exceptions however, as for example in South Africa, where impala (Aepyceros melampus), hartebeest (Alcelaphus spp) and wildebeest (Connochaetes taurinus) were said to have escaped. Since that pandemic all reported occurrences of rinderpest in wildlife have been in the equatorial region of central and eastern Africa with a single incident in 1983 in Nigeria (Shathikumar et al., 1985). The species most commonly affected were buffalo (sylzcerus caffer) , eland ( Taurotragus oryx) and warthog (Phacuchuerus aethiupicus) . From this history it was possible to draw up a list of species in order of susceptibility and such a list has been published (Plowright, 1982). The incidence of rinderpest has been much reduced since the introduction of the Pan African rinderpest campaign (PARC) at the beginning of 1985. Eradication of the disease from Africa is the goal and this has already resulted in the large populations of wildlife becoming susceptible once more. There is again the potential for epidemics involving wildlife populations where even the smaller populations of the putatively less susceptible species could be significant in epidemiological terms. Should this occur there could be significant mortality in some species. Species occurring on the Indian subcontinent reported as being susceptible are given in Table 1. PPR Almost nothing is known about the occurrence of PPR in African wildlife although the virus is now present in north-east, west and east Africa. The only report has been that of Furley et al. ( 1987) who reported that Dorcas gazelle (Gazella dorcas) and gemsbok ( Oryx gazella) held in a zoological collection in the Arabian Gulf died. Nilgai (Boselaphus tragocamelus) were also subclinically affected. Presumably all the antelope species are potentially susceptible for PPR. Some species occur in very large numbers (Figs. 34) while others such as the gazelle (Gazella spp.), bushbuck (Tragelaphus scriptus), impala, and duiker ( Cephalophus spp), although not occurring in large numbers, are very widely distributed throughout the region and occur in most of the pastoral areas alongside sheep and goats. This suggests that PPR infection in antelope might become of much greater significance in the future. This could also apply to the Middle East where significant populations of some antelope species still occur in the nomadic pastoral areas.
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Mara Serengeti Tsavo Ngorongoro Tarangire Mikumi Rungwa Kilombero Ruaha Katavi Selous National
BUFFALO Source
AND - SWRI
Fig. 2. Distribution
Parks
and
wildlife
WILDEBEEST
Buffalo
Wildebeest
2.000 43. 546
1. 146. 000
1. 963
il. 847
23. 816 12.410 t3.393
12. 474 -
24. 197
59. 261 31. 263 93. 792 157. 536
63. 202
areas
POPULATION
DENSITIES
- EAST AFRICA
report 1988 and density of buffalo and wildebeest populations
in East Africa.
3. Population biology Of central importance for the establishment, persistence and spread of microparasites to other species is the magnitude of the basic reproductive rate (Anderson and May, 1986; Anderson, 1991). Its principal determinants are host density and birth rate. The critical host density for rinderpest is determined by the relative susceptibility of the species and the virulence of the infecting virus strain. For morbillivirus infections, which are horizontally transmitted and give rise to a lasting immunity in surviving animals, the critical host density is large. The basic reproductive rate of rinderpest virus in wildlife populations is also increased where the probability of transmission by contact is greatest i.e. in species which form herds (buffalo, wildebeest, white-eared kob (Kobus spp.) , tiang (Damdiscus spp.) and which migrate (wildebeest, white-eared kob) . The reproductive rate is decreased where the infecting strain is highly virulent or the infected species is very susceptible resulting in high mortality, when the infecting strain is mild or the species has an innate resistance and also in adverse conditions such as drought and when there is high predation or poaching and human encroachment. With these principles in mind the population biology of the most susceptible and abundant species will be considered in relation to distribution, population density and population dynamics (movement/range; behaviour, i.e. herds or solitary; and reproductive rate). 3.1. Distribution The current distribution of buffalo in East Africa is shown in Fig. 2 and those of the antelope in eastern Africa in Figs. 34. These clearly indicate the large concentrations of susceptible species that are distributed throughout this region which could, theoretically, act either as reservoirs of infection or contribute to the spread of the disease. In spite of these very large populations of wild herbivores, the disease disappeared from the wildlife populations of northern Tanzania in the early 1960s and was not sustained in
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44 (1995) 319-332
AND IOW 60.000 -36.000 10. 000 70.000 13.800 10.000 4.500
TRAGELAPHINES
GAZELLE
Fioan/Sable)
Source:
East.1998.
Fig. 3. Distribution and density of wildebeest, East Africa (data from East, 1988).
IUCN Antelope
eland, gazelle (Thomsons
survey.
and Grant), roan and sable antelope in
the wildlife there following its recurrence in buffalo in this region in the early 1980s (Anderson et al., 1990). In view of the fact that these wildlife populations are increasingly encroached upon by the expanding human populations, it seems unlikely that they would act as a reservoir of rinderpest infection in the future. However, were it to be re-introduced from cattle, they could be significant in amplifying the virus and contributing to its spread. SUDAN
u
Tiang
Uganda kob ?
#
White-eared e50.000
714.000 kob
-
Giant
eland
18. 000 common
Lelwal
hartebeast
eland
io.000 &#z
Source:
East, 19EB -1UCN
Fig. 4. Distribution and density of White-eared Sudan (data from East, 1988).
and Uganda kob, tiang, eland, lechwe and hartebeest in southern
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3.2. Population density Rinderpest can establish infection in relatively small populations of susceptible species but large populations are necessary for infection to be sustained. A classic example of this was the presence of enzootic disease between the 193Os-1964 in the large concentrations of wildlife in north Tanzania (Plowright, 1982). Highly virulent strains will theoretically require larger populations in order to persist than strains of lower pathogenicity (Rossiter and James, 1989). It is only in Africa that sufficiently large numbers of susceptible wildlife occur to be of significance in the epidemiology of rinderpest. Population densities in the Middle East and India are likely to be too small. 3.3. Movement/range The range or migratory habits of each species determines the contact rate between herds of either the same or different species and therefore has an important bearing on the transmission potential of each species. There are two examples where very large numbers of animals migrate in a seasonal pattern over a large area. These are the wildebeest population ( 1.2 million) of the Serengeti ecosystem (Figs. 2-3) and the white-eared kob ( 850 000) in the Nile region of southern Sudan (Fig. 4). Such large populations have theoretically the potential to sustain the virus and spread it to other animals. However, as already stated, rinderpest disappeared from the Serengeti wildebeest populations in 1964 (Plowright, 1982) and the disease has never been reported in the large herbivore populations of southern Sudan. The reasons for this are unclear. The other species that may range quite widely but which is not as numerous is the eland (Fig. 3). This is a very susceptible species in which infection will be able to establish itself. Populations are too small for this species to sustain infection but it could, theoretically at least, contribute to the spread of infection. 3.4. Behavioural patterns Morbillivims infections require close contact for transmission to occur and therefore transmission is more likely in species which form herds such as buffalo, wildebeest, kob and eland. The contact rate between solitary animals, such as bushbuck and duiker as well as those which only form small groups such as giraffe (Giraffa camelopardalis), topi (Damaliscus korrigum) , warthog, impala, roan (Hippotragus equinus), sable (Hippotragus niger), waterbuck (Kobus ellipsiptymnus) and kudu ( Tragelaphus spp.) is much lower. 3.5. Reproductive rate The net birth rate determines whether infection is simply established or whether it is able to persist (Anderson and May, 1986). Factors that affect this in wildlife populations include climate (drought causes significant losses in newborn animals) predators and diseases affecting reproduction (bovine viral diarrhoea, brucellosis) or causing debility (tuberculosis). In the higher rainfall belts of the rinderpest enzootic region of Africa some wildlife species give birth over an extended period while others, such as the impala, have two distinct
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44 (199.5) 319-332
37.5
k_/,--&d’ Fig. 5. Distribution
of African buffalo (from Lessard et al.. 1990)
annual breeding seasons. Buffalo calves in the Serengeti, for example, are born between December and July each year and therefore susceptible young animals are present throughout the year in this and other similar areas. Calving in wildebeest populations is more seasonal and takes place once a year but the calving period extends over several months. Such is also the case with the tiang and kob in southern Sudan and Uganda. In these situations, should the initial herd immunity, through the presence of enzootic disease, be low or should the infecting strain be of low virulence, and as the herd size is sufficient, it would theoretically be possible for such a seasonality of calving to allow the persistence of infection (Rossiter and James, 1989). The recruitment rate for any population is approximately twenty percent per year. Although predators will account for some of this there is a very significant number of young susceptibles present in an enzootic area.
4. Consideration
of the significance
of some individual
species
4.1. Buffalo (syncerus cafser) Buffalo are still widely distributed throughout equatorial Africa (Fig. 5). This distribution coincidentally is similar to the rinderpest endemic regions. The densities of different pop-
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Buffalo populations in 4 regions of Serengeti Number 30,CilO
0 North
West
Southwest
From: Serengeti Wildlife Research Centra Report 1930-92
Fig. 6. Buffalo populations
in the Serengeti National Park.
ulations are only currently known with any accuracy for eastern Africa (Fig. 2). In Kenya buffalo are widely distributed occurring in Laikipia district, in the Mt Kenya and Aberdare forests, Tana river, the Tsavo Nationai Park and in the Mara National Park which forms the northern tip of the Serengeti ecosystem. The population is estimated at 17-35 000 (R. Kock, personal communication). These populations are large enough and wide enough in their distribution to allow the establishment of infection and to contribute to the dissemination of the disease but not large enough to sustain it. In Tanzania the total buffalo population numbers about 500 000 and is also widely distributed. The largest concentration occurs in the Selous Game reserve but there are significant numbers in all the other areas. Apart from the tsetse infested areas of west and south Tanzania there are also significant populations of domestic animals in all these areas. Again it is doubtful if any single population would be large enough to maintain rinderpest infection on its own. It was estimated that a population of half a million would be required for measles to persist in a human population (Black, 1975). It was in the Serengeti ecosystem of northern Tanzania and southern Kenya that rinderpest became endemic in the late 1920s and remained so until 1964. There are four distinct buffalo populations in the Serengeti National Park (Fig. 6) that occur in the north, west, central and south-west. These populations are separated by quite large distances devoid of buffalo. The range of any buffalo herd does not exceed a radius of some 50 km and in the Serengeti contact between these populations does not occur. Even between contiguous herds, contact may be transitory (Sinclair, 1977). Following the outbreak of rinderpest in buffalo in the north of the Serengeti in 1982 and deaths of buffalo and eland in the Ngorongoro conservation area, a serological survey was carried out between 1987-1989 (Anderson et al., 1990) which showed that buffalo in the Tarangire National Park had also been infected (Fig. 7). The question of how infection spread between these discrete buffalo populations remains open. In the Serengeti, was it via the vast migratory wildebeest population or
321
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L.
Victoria
TANZANIA
A
LOCATIONS
OF SEAO-POSITIVE
Fig. 7. Places in northern Tanzania outbreak of the disease in 1982.
BUFFALO
where buffalo positive for rinderpest
antibody
were found following
the
perhaps by the widely distributed and wide ranging eland population? Did the surrounding nomadic cattle population play a part? Unfortunately, these populations were not investigated. The disease, however, did not persist in these populations (Anderson et al., 1990) and there is no evidence that it spread to buffalo populations in southern Kenya (Rossiter, personal communication). 4.2. Wildebeest (connochaetes
taurinus)
The importance of this species, which occurs in vast numbers ( 1.2 million) in northern Tanzania and southern Kenya (Figs. 2-3), has been appreciated since the 1920s. The numbers of wildebeest in the Serengeti have risen markedly over the last 20 years (Fig. 8) increasing their potential as a reservoir of infection. There are also some 63 000 present in the Selous game reserve in the south of Tanzania. The large population in the Serengeti should theoretically be able to sustain rinderpest infection. This has not occurred (Plowright, 1982), possibly due to the innate resistance that this species has to infection. 4.3. Eland (taurotragus
oryx)
The wide distribution of eland is shown in Figs. 3-4 and they also occur in significant numbers. In Tanzania there are about 60 000 eland (Serengeti-13 813; Rukwa Ruaha5000; Tabora-1800; Tarangire-Simanjiru-10 000; Selous-5-11 000). In Kenya their numbers are estimated at 50 000-60 000. In southern Sudan there are an estimated 10 000 common eland and 18 000 giant eland (East, 1988). Eland form herds of 20 to 80 individuals. They may range over an area of up to 100 km*. They also occur in habitats frequented by domestic animals as well as in the wildlife areas of the region. The densities of individual
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Serengeti Population
44 ( 1995) 319-332
Wildebeest Population (millions1
Estimates
2
1965
1955
m Serengeti
1975
Wildlife
zebra
pl
wildebeest Research
Fig. 8. Increase in the wildebeest population
1989
19e5
YEAR Centre
Report
1988-89
of the Serengeti National Park since 1955.
populations are insufficiently large to maintain infection could contribute to the dissemination of the disease.
but, as mentioned
above, they
4.4. White-eared kob, tiang and hartebeest
All these species occur in very large numbers be able to sustain persistent infection. It is known rinderpest in 1929-193 1 (Scott, 1981) but there in the larger populations of white-eared kob, tiang
in southern Sudan (Fig. 4), sufficient to that the Uganda kob were decimated by is no record of rinderpest ever occurring and Lelwel hartebeest in southern Sudan.
4.5. Overall perceived signijicance of African artiodactyla in the epidemiology of rinderpest Combining what is known about the relative susceptibility of different species, and taking into account those aspects of their population biology discussed above, the likely significance of each wildlife species in any future outbreaks of rinderpest in Africa is shown in Table 2.
5. Canine distemper 5.1. Susceptibility of terrestrial species This subject is addressed by Appel and Summers ( 1995). Species reported to be susceptible (Budd, 198 1) are listed in Table 3. The disease was responsible for the extirpation of the black-footed ferret (Mustela nigripes) from the wild (Thome and Williams, 1988). The disease has also been reported in the black-backed jackal ( Canis mesomelas) (Moehl-
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44 (I 995) 319-332
Table 2 The perceived significance of members of the Order Artiodactyla, taking into account their relative susceptibility and their population dynamics, in the maintenance and spread of rinderpest Species
Susceptibility
Density and Distribution
Buffalo (Swrcerus caffer) Wildebeest (Connochaetes taurinus) Eland (Taurotragus oryx) Kob (Kobus kob thomasi, leucotis) Giraffe (Giraffa camelopardalis) Warthog (Phacochoerus aethiopicus)
+++ ++ +++ +++ ++ +++ ++ ++ +++ ++ ++ ++ ++ + ++ ++ ++ + + + +/-
+++ +++ ++ ++ ++ + ++ ++ + + + + + ++ + + + + + + + + +
Oryx (Oryx gazella)
Topi (Damaliscus korrigum) Kudu (Tragelaphus spp. ) Bushbuck (Tragelaphus scriptus) Reedbuck (Redunca spp. ) Sitatunga (Tragelaphus spekei) Bushpig (Potamochoerus porcus) Impala (Aepyceros melampus) Waterbuck (Kobus ellipsiprymnus) Roan (Hippotragus equinus) Sable (Hippotragus niger) Duiker (Cephalophus sp. ) Oribi (Ourebia) Steinbok (Raphicerus campestris) Hartebeest (Alcelaphus spp.) Hippopotamus (Hippopotamus amphibus) Gerunuk (Litocranius walleri)
+I+/-
man, 1983), the bat-eared fox (Otocyon megalotis), mongoose ( Viuerridae) and hyaena ( Crocuta crocuta) (Plowright, 1988), the masked palm civet (Paguma Zarvata) (Machida et al., 1992) and coyotes (Canis Iatrans) (Gese et al., 1991). In a study on the causes of mortality in grey foxes ( Urocyon cinereoargenteus) in east-central Alabama, Nicholson and Hill ( 1984) reported that 35 percent were due to distemper. Isolation of morbilliviruses has also been reported from red squirrels (Sciuris uulgaris) (Vizoso, 1968) and hedgehogs (Erinaceus europaeus) (Vizoso and Thomas, 198 1) . Table 3 Species in the order Camivora
reported to be susceptible
to canine distemper
Family
Species
Canidae Mustelidae Procyonidae Vivemidae Protelidae’ Hyaenidae * Felidae * Viverridae *
foxes, wild dog, jackal, dingo, coyote, wolf weasel, ferret, mink, badger, stoat, martin kinkajou, racoon. panda, coati civet aardwolf hyaena lion genet, mongoose
* Species possibly susceptible
to canine distemper but insufficient evidence.
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More recently there have been serious outbreaks of canine distemper in captive lion (Pa&era Zeo), tiger (P. tigris), leopard (P. par&s) and jaguar (P. onca) in California and in free-ranging lion in the Serengeti National Park in Tanzania ( Appel and Summers, 1995). The possibility that mustelids act as reservoirs of infection for dogs in Germany is discussed by van Moll et al. ( 1995). 5.2. Population
biology
Distribution and density Susceptible species are generally widely distributed. They occur singly, in pairs or in groups, as for example with the Cape hunting dog (Lycaon pictus) where groups average 8-12 individuals though they can contain up to 35 dogs. Bat-eared fox form groups of up to 15 when feeding. How the disease was introduced to the lion population of the Serengeti remains to be determined but there was sufficient contact within the lion population to allow the spread of the disease which has resulted in a high mortality rate. Range Most species have a limited range but there are exceptions as with the Cape hunting dog which ranges over an area of 1,500-4000 km* in the Kruger National Park in South Africa and over a range of 450 km* in East Africa (Skinner and Smithers, 1990). Reproductive rate This can be quite significant on an individual basis. Thus the Cape hunting dog will have 2-19 pups. However the average litter size of the bat-eared fox is four while that of the black-backed jackal is only two. This latter figure reflects more closely the reproductive rate of the group as a whole which is therefore not large.
6. Conclusions Sufficient densities of wildlife to sustain rinderpest in the enzootic regions of Africa presently exist only in eastern Africa. These wildlife populations are totally susceptible to rinderpest. If a virulent strain were again to be introduced to these populations they would, in all probability, once more be decimated. Less virulent strains would probably also result in significant losses. There is, however, no evidence to support the theory that these wildlife species would remain as reservoirs of rinderpest infection. The fact that the disease was unable to maintain itself after 1964 in the large wildlife populations of northern Tanzania following control of the disease in cattle supports this. Rinderpest has never been reported in the large wild herbivore populations of southern Sudan. There are probably insufficient numbers of susceptible wildlife species in either the near East or India to be of significance. With regard to PPR very little is known about its ecology in wildlife. It is a disease that is more difficult to detect, which causes mild infections in the very large and widely distributed populations of small domestic ruminants, and one at which no control measures
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331
are currently directed. It is possible that it will become endemic in Africa’s wildlife if it has not already done so. Canine distemper will continue to be of significance in the endangered susceptible wildlife species and in zoological collections but its occurrence in wildlife has little or no significance for its control in domestic animals.
Acknowledgements I would like to thank Dr Brian Perry and Dr Russ Kruska of the International Laboratory for Research on Animal Diseases (ILRAD), Nairobi for providing the figure on buffalo distribution in Africa.
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