Download Diseases of wild animals transmissible to domestic animals

Rev. sci. tech. Off. int. Epiz., 1988, 7 (4), 705-736.
Diseases of wild animals transmissible
to domestic animals
P.-P. PASTORET, E. THIRY, B. BROCHIER, A. SCHWERS,
I. THOMAS and J. DUBUISSON *
Summary: The authors have reviewed reports submitted by 22 Member Countries
of the OIE concerning diseases of wild animals transmissible to domestic animals,
and have outlined the main trends. It is emphasised that many infections and
infestations are specific and are not transmitted from wild to domestic species.
Diagnostic and epidemiological tools are often unsuitable, and false conclusions
may be drawn from their results. While attention may be focussed on the
transmission of certain diseases from wild to domestic animals, the reverse also
applies, particularly in view of the considerable improvement in the economic
status and cultural appreciation of wild animals in recent years. In some cases,
intervention may be necessary to improve the health of wild species, particularly
in disturbed ecological systems.
Certain diseases are selected for detailed consideration because of their
importance, such as malignant catarrhal fever, African swine fever, foot and
mouth disease (in Africa), African horse sickness and pestiviral infections.
The authors conclude that it is necessary to reshape thinking in veterinary
circles concerning the approach to disease problems created by wildlife. The
role played by wildlife must be reconsidered, and specific research programmes
must be initiated to develop more suitable diagnostic, epidemiological and
conceptual tools.
KEYWORDS: Animal diseases - Animal resources - Animal welfare - Disease
control - Disease transmission - Domestic animals - Ecosystems - Epidemiology Game ranching - Veterinary research - Wild animals - Zoonoses.
INTRODUCTION
The problem created by diseases of wild animals transmissible t o domestic animals
is complicated for many reasons.
Firstly, the infections or infestations which m a y be exchanged are relatively
numerous and of various types, comprising viral, bacterial a n d parasitic diseases.
Some of them are also transmissible t o m a n , which further complicates the problem.
Next, the economic, geographical and ecological situations which permit reciprocal
transmission are extremely variable, as is also the degree of intensification of animal
* Département de Virologie-Immunologie, Faculté de Médecine vétérinaire de l'Université de Liège,
45, rue des Vétérinaires, B-1070 Brussels, Belgium.
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production, whether in domestic or wild species. T h e extent of surveillance and
diagnostic activities is also varied.
Finally, whereas a situation may be relatively simple from the aspect of
domesticated species, the same may not apply to the wild species, given the differences
in their variety and population density.
The problem is complicated further because certain wild species are bred in
captivity under ranching or farming conditions. Examples can be cited in industrialised
countries (such as deer in Scotland) and in African countries (such as Zimbabwe).
Certain wild species may be introduced into a country for subsequent release or
maintenance in captivity, and this creates difficulties from the aspect of international
t r a d e . Others may be bred in order t o repopulate game reserves. In recent years these
aspects have become quite important, and so they will be dealt with separately in
this report.
It should be noted that the problem does not flow in one direction only, so that
in addition t o considering the risks posed by wildlife for domestic animals, it is also
necessary to consider domestic species as sources of risk to wildlife. The most striking
example of the latter is the spread of rinderpest throughout the African continent
at the end of the last century (108, 89), and its often dramatic extension t o big game.
Fortunately, examples as spectacular as this are rare, and it is true to say that,
although the infections or infestations shared by wildlife and domestic animals a n d / o r
m a n are n u m e r o u s , they are still a minority. In fact, most infections (particularly
viral diseases and parasitoses) are not shared but are strictly specific, being confined
to a single species or to closely related species.
The specificity of infections and infestations has not always been recognised, and
even today prophylactic measures sometimes fail to take it into account. This raises
a special problem which will be dealt with later in this report. The specificity of
infections is well illustrated by the case of Australia, where problems arise not from
the indigenous mammals (marsupials) but from introduced placental mammals which
have reverted to the feral state. In addition, it is unfortunate that there is often little
knowledge of the actual susceptibility of wild species to the pathogens of domestic
animals.
This report commences with a review of information provided by twenty-two
Member Countries (or territories) of the O I E and placed at our disposal by that
organisation. It continues with an account of problems selected because of their
importance, and of diseases which play a major role.
It ends with a concise summary of the information, general conclusions and several
recommendations. The complexity of the problem is such that it is impossible to
provide an exhaustive account within the limited extent of this review. Our presentation
is thus confined to an outline of the essential features.
LIST OF T H E P R I N C I P A L DISEASES C O N S I D E R E D
Table I shows the principal diseases mentioned in the various reports, together
with the country supplying the information and the wild species which may act as
source.
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It is regrettable that few of the reports use the internationally accepted Latin names
of species. In some cases it has proved difficult to define the species involved simply
from the vernacular n a m e .
The diseases are classified according to List A and List B of the O I E . W e have
added a third list for information concerning infections not usually contained in the
official lists.
TABLE I
Principal diseases, countries
affected
and susceptible wild species
Disease name
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
LIST A DISEASES
Foot and mouth
disease
Uganda
African buffalo (Syncerus caffer)
South Africa
African
Impala
Greater
African
African
Zambia
Zimbabwe
Bulgaria
Switzerland
USSR
Vesicular
stomatitis
Rinderpest
buffalo (Syncerus caffer)
(Aepyceros melampus)
kudu (Tragelaphus strepsiceros)
buffalo (Syncerus caffer)
buffalo (Syncerus caffer)
Wild boar (Sus scrofa) in 1960
Saiga antelope (Saiga tatarica)
A zoonosis
USA
Feral pigs, wild boar (Sus scrofa) and
other species
Uganda
African buffalo (Syncerus caffer)
Warthog (Phacochoerus aethiopicus)
Species particularly susceptible:
African buffalo (Syncerus caffer)
Warthog (Phacochoerus aethiopicus)
Eland (Tragelaphus oryx)
Greater kudu (Tragelaphus strepsiceros)
Very susceptible species:
Bushbuck (Tragelaphus scriptus)
Bush pig (Potamochoerus porcus)
Giraffe (Giraffa camelopardalis)
Sitatunga (Tragelaphus spekei)
Bongo (Tragelaphus euryceros)
Gnu (Connochaetes spp.)
Giant forest hog (Hylochoerus
meinertzhageni)
South Africa
708
T A B L E I (contd.)
Disease name
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Rinderpest
(contd.)
South Africa
(contd.)
Togo
Moderately susceptible species:
Reedbuck (Redunca spp.)
Tsessebe or topi (Damaliscus lunatus)
Blesbok (Damaliscus dorcas albifrons)
Bontebok (Damaliscus dorcas pygargus)
Gemsbok (Oryx gazella)
Roan antelope (Hippotragus equinus)
Sable antelope (Hippotragus niger)
Oribi (Ourebia ourebi)
Impala (Aepyceros melampus)
Springbok (Antidorcas marsupialis)
Species not very susceptible:
Common Waterbuck (Kobus
ellipsiprymnus)
Duikers (Cephalophus spp.)
Beisa oryx (Oryx beisa)
Grant's gazelle (Gazella granti)
Dik-dik (Madoqua spp.)
Red hartebeest (Alcelaphus buselaphus)
Fairly resistant species:
Thomson's gazelle (Gazella thomsoni)
Hippopotamus (Hippopotamus
amphibius)
Gerenuk (Litocranius walleri)
African buffalo (Syncerus caffer)
South Africa
Absent in wildlife
Lumpy skin
disease
Rift Valley
fever
Bluetongue
A zoonosis
South Africa
African buffalo (Syncerus caffer)
Springbok (Antidorcas marsupialis)
Blesbok (Damaliscus dorcas albifrons)
Monkeys and rodents
Serological evidence in: hippopotamus
(Hippopotamus amphibius) and the
African elephant (Loxodonta africana)
South Africa
Specific antibodies are present in most
African artiodactylids, African
elephant (Loxodonta africana) and
various rodents
White-tailed deer (Odocoileus
virginianus)
Mule deer (Odocoileus hemionus)
Often confused with epizootic
haemorrhagic disease of Cervidae
Feral cattle and water buffalo
USA
Australia
709
T A B L E I (contd.)
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
African horse
sickness
South Africa
Zebra (Hippotigris)
African swine
fever
Uganda
Disease name
South Africa
Zambia
Zimbabwe
Classical swine
fever
Fowl plague
Warthog (Phacochoerus aethiopicus)
Bush pig (Potamochoerus porcus)
Soft tick (Ornithodoros moubata)
Warthog (Phacochoerus aethiopicus)
Bush pig (Potamochoerus porcus)
Giant forest hog (Hylochoerus
meinertzhageni)
Warthog (Phacochoerus aethiopicus)
Bulgaria
USSR
Wild boar (Sus scrofa)
Australia
New Caledonia
United Kingdom
Surveillance of wild birds
Surveillance of wild birds
Aquatic birds
Newcastle
disease
A zoonosis
USA
Australia
New Caledonia
France
United Kingdom
Sweden
USSR
Surveillance of birds
Surveillance of birds
Serological evidence of infection in
wild birds
Surveillance of birds
Semi-domesticated pigeons
(Columba livia)
Semi-domesticated pigeons
(Columba livia)
Semi-domesticated pigeons
(Columba livia)
Wild birds
LIST B DISEASES
Anthrax
Aujeszky's
disease
A zoonosis
South Africa
Disease particularly spread by flies;
rare species in game parks, such as
the roan antelope (Hippotragus
equinus), are vaccinated
USA
Feral pigs
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T A B L E I (contd.)
Disease name
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Aujeszky's
disease (contd.)
Mexico
USSR
Wild boar (Sus scrofa)
Echinococcosishydatidosis
A zoonosis
Australia
Bulgaria
Portugal
Switzerland
USSR
Heartwater
South Africa
Zimbabwe
Leptospirosis
Typical cycle between domestic dogs
and sheep, also a wildlife cycle in
dingoes, stray dogs and the kangaroo
family (Macropodidae)
Fox (Vulpes vulpes)
Wolf (Canis lupus)
Wild boar (Sus scrofa)
Carnivores
Tick-transmitted; tortoises may serve
as a sylvatic reservoir by harbouring
early stages of the vector,
Amblyomma hebraeum. No
information on the role of wild
ungulates; infection is asymptomatic
in blesbok (Damaliscus dorcas
albifrons)
Eland (Tragelaphus oryx) may act as
a reservoir
A zoonosis
Mentioned by many
countries and stressed by
some; complex situation
because of the number of
different serotypes
Cuba
Rat and deer
Australia
Feral pigs, feral cattle, water buffalo,
deer and certain indigenous species,
such as wombat
Republic of Korea
Voles and rats
New Caledonia
Mice, timor deer
France
Rodents, hedgehog (Erinaceus
europaeus)
United Kingdom
Brown rat (Rattus norvegicus) and
other wild species
Sweden
Hedgehog (Erinaceus europaeus)
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T A B L E I (contd.)
Disease name
Country which
provided
information
Q fever
South Africa
France
Switzerland
Rabies
Uganda
South Africa
Zambia
Zimbabwe
USA
Mexico
Bulgaria
Switzerland
USSR
Anaplasmosis,
babesiosis,
toxoplasmosis
and other protozoal
infections
Wildlife species
and (when applicable)
susceptibility of man
A zoonosis
Tick-transmitted, perhaps with a
wildlife cycle
High serological prevalence in the roe
deer (Capreolus capreolus)
Game animals and small wild
mammals act as reservoirs; roe deer
(Capreolus capreolus) are involved
directly
A zoonosis
Stray dogs, black-backed jackal
(Canis mesamelas)
Stray dogs, yellow mongoose (Cynictis
penicillata), black-backed jackal
(Canis mesomelas), wild cats (Felis
spp.), genet (Genetta), greater kudu
(Tragelaphus strepsiceros), feral cat,
ratel (Mellivora capensis), bat-eared
fox (Otocyon megalotis), meercat
(Suricata suricata).
Rabies has been diagnosed in 36 wild
species, of which the following have
an epidemiological role: yellow
mongoose, black-backed jackal, wild
cat, genet, meercat, bat-eared fox and
greater kudu
Fox, jackal, ratel (Mellivora capensis),
mongoose, etc.
Stray dogs, jackals
Vampire bats (Desmodus rotundus) are
responsible for paralytic rabies in cattle
Fox (Vulpes vulpes)
Stray dogs, fox (Vulpes vulpes),
golden jackal (Canis aureus), wolf
(Canis lupus), raccoon-dog
(Nyctereutes procyonoides)
South Africa
Complex situation; toxoplasmosis
associated with cats (a zoonosis)
Australia
Bulgaria
Sweden
Toxoplasmosis associated with feral cats
Toxoplasmosis in hares
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T A B L E I (contd.)
Disease name
Country which
provided
information
Paratuberculosis
USA
Brucellosis
South Africa
Cuba
USA
Mexico
Australia
Bulgaria
France
Switzerland
USSR
Tuberculosis
South Africa
Zambia
Cuba
USA
Australia
Wildlife species
and (when applicable)
susceptibility of man
A zoonosis
African buffalo (Syncerus caffer),
hippopotamus (Hippopotamus
amphibius); wild animals are not
reservoirs, but are infected by
domestic animals
Feral pigs
Bison (Bison bison), wapiti (Cervus
canadensis), white-tailed deer
(Odocoileus virginianus), fur-bearing
animals; feral pigs have been
examined for brucellosis
Feral cattle and feral pigs
Hares (Lepus capensis) infected with
Brucella suis
Hares (Lepus capensis) introduced for
repopulation, infected with Brucella suis
Saiga (Saiga tatarica) infected with
B. melitensis; hares (Lepus capensis),
wild boar (Sus scrofa)
A zoonosis
Wildlife infection from contact with
man and domestic animals.
Diagnosed in: African buffalo
(Syncerus caffer), greater kudu
(Tragelaphus strepsiceros), common
duiker (Cephalophus grimmia), lechwe
(Kobus leche); all isolates have been
Mycobacterium bovis.
M. bovis, M. avium and
M. tuberculosis (human) have been
isolated from many species kept in
zoos, including monkeys and elephants
Wild ruminants
Diagnosed in zoos
Axis deer, feral pigs, mongooses and
wild goat are under surveillance on
Molokai Island (Hawaii)
Water buffalo, feral pigs and feral cattle;
marsupials seem to be infected rarely
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T A B L E I (contd.)
Disease name
Tuberculosis
(contd.)
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Taiwan R.O.C.
Finland
United Kingdom
Farmed deer
Wild birds
Badgers (Meles meles) act as wildlife
reservoir for bovine tuberculosis
(M. bovis), and 10% are infected in
certain areas. In regions where
badgers are present, roe deer
(Capreolus capreolus) and sika
(Sika nippon) may become infected;
also red deer (Cervus elaphus)
introduced into the country. M. bovis
recovered from rat, fox (Vulpes
vulpes), mole (Talpa europaea) and
mink
Sweden
Switzerland
Birds a possible source of M. avium
M. avium from pigeons and birds of
prey. M. bovis has disappeared from
game animals following eradication of
the disease in cattle
M. avium and M. bovis isolated from
wild birds. Infection may be present
among wild boar (Sus scrofa) and red
deer (Cervus elaphus)
USSR
Dermatophilosis
(Senkobo skin
disease)
South Africa
Occurs in eland (Tragelaphus
oryx), giraffe (Giraffa
camelopardalis), Thomson's gazelle
(Gazella thomsoni), zebra
(Hippotigris), greater kudu
(Tragelaphus strepsiceros), roan
antelope (Hippotragus equinus), sable
antelope (Hippotragus niger).
It is hard to discover the true source
of infection
Infectious
bovine
rhinotracheitis
South Africa
Specific antibodies occur in 14
wild species, including African
buffalo (Syncerus caffer), eland
(Tragelaphus oryx), brindled gnu
(Connochaetes taurinus), common
Waterbuck (Kobus ellipsiprymnus),
reedbuck (Redunca spp.), hippopotamus
(Hippopotamus
amphibius).
The virus has been isolated from gnu.
See the comments in the chapter on
herpesvirus infections
Switzerland
Wild animals play no part in infecting
domestic animals
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T A B L E I (contd.)
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Theileriasis
South Africa
Zimbabwe
No comments received
Theileria parva lawrenci in African
buffalo (Syncerus caffer).
Vectors are Rhipicephalus
zambesiensis and R. appendiculatus
Trichomoniasis
Australia
Occurs among feral cattle
Disease name
Trypanosomiasis
Uganda
South Africa
Zambia
A zoonosis
Wild animals are a source of
infection; tsetse fly vector
Mainly T. congolense and T. vivax in
cattle, T. brucei in horses and
T. simiae in pigs. 60% of cases of
infection are attributable to wild pigs
and 35% to wild ruminants as
follows: 10% for African buffalo
(Syncerus caffer) and 25% for eland
(Tragelaphus oryx), greater kudu
(Tragelaphus strepsiceros) and
bushbuck (Tragelaphus scriptus)
combined; the African elephant
(Loxodonta africana) accounts for
only 5%
Species encountered: T. congolense,
T. vivax, T. brucei, T. zambesiensis
Zimbabwe
Venezuelan equine
encephalomyelitis
A zoonosis
USA
Surveillance of wild birds and rodents
was conducted in Texas in 1971
Mexico
Trichinellosis
USA
Bulgaria
Finland
Portugal
United Kingdom
Sweden
Switzerland
USSR
A zoonosis
Feral pigs
Brown bear (Ursus arctos)
Wild boar (Sus scrofa)
Wild carnivores
Wild boar (Sus scrofa)
Rat and fox (Vulpes vulpes)
Fox (Vulpes vulpes) and badger
(Meles meles)
Fox (Vulpes vulpes)
Reservoirs are: wolf (Canis lupus),
fox (Vulpes vulpes), wild boar
(Sus scrofa), badger (Meles meles),
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T A B L E I (contd.)
Disease name
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Trichinellosis
(contd.)
USSR
(contd.)
raccoon-dog (Nyctereutes
procyonoides), bear (Ursus arctos),
arctic fox (Alopex lagopus), marine
mammals
Duck virus
enteritis
United Kingdom
Wild ducks, particularly mallard
(Anas platyrhynchos)
Psittacosisornithosis
A zoonosis
France
USSR
Psittacides in captivity: semidomesticated pigeons (Columba livia)
Wild birds infected; diagnosed in
domestic ducks and turkeys
Pigeons and sparrows
Myxomatosis
Australia
France
Portugal
Switzerland
Rabbit destruction campaigns
Wild rabbit (Oryctolagus cuniculus)
Wild rabbit (Oryctolagus cuniculus)
Wild rabbit (Oryctolagus cuniculus)
Tularaemia
Bulgaria
Finland
USSR
United Kingdom
Leishmaniasis
South Africa
Hares (species not given)
Common vole (Microtus arvalis),
water vole (Arvicola amphibius),
muskrat (Ondatra zibethicus)
A zoonosis
Hyrax (Procaviidae)
OTHER DISEASES NOT LISTED IN THE TWO PREVIOUS CATEGORIES
Malignant
catarrhal
fever
South Africa
With intensification of the
rearing of game animals, this
disease has become the most
important cause of death of big game.
Both white-tailed and brindled gnu
(Connochaetes gnou, C. taurinus) act
as asymptomatic carriers.
The virus has also been isolated from
red hartebeest (Alcelaphus buselaphus)
and tsessebe (Damaliscus lunatus) but
there is no evidence of transmission.
All Cervidae and Bovidae are
susceptible, excepting perhaps the
African buffalo (Syncerus caffer).
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T A B L E I (contd.)
Disease name
Country which
provided
information
Wildlife species
and (when applicable)
susceptibility of man
Malignant catarrhal
fever (contd.)
South Africa
(contd.)
Eland (Tragelaphus oryx) and giraffe
have been infected experimentally.
The European sheep-associated form
also occurs
Brindled gnu (Connochaetes taurinus)
Imported deer living in the wild state
Zimbabwe
Australia
Herpesvirus
mammillitis
(Allerton herpesvirus
infection)
South Africa
Known to occur in African buffalo
(Syncerus caffer); virus isolated.
A serological survey showed that
nearly all buffalo were infected;
antibodies also present in giraffe
(Giraffa camelopardalis), Waterbuck
(Kobus ellipsiprymnus), hippopotamus
(Hippopotamus amphibius), eland
(Tragelaphus oryx), oryx (Oryx
gazella), impala (Aepyceros
melampus), bushbuck (Tragelaphus
scriptus) and gnu (Connochaetes spp.)
Ephemeral fever
South Africa
54% of African buffalo (Syncerus
caffer) serologically positive, also 62%
of Waterbuck (Kobus ellipsiprymnus),
9% of gnu (Connochaetes spp.) and
2.8% of red hartebeest (Alcelaphus
buselaphus)
Water buffalo, feral cattle and deer
introduced into Australia
Australia
Contagious ecthyma
A zoonosis
Switzerland
Mange
Australia
Bulgaria
Finland
Portugal
Sweden
Listeriosis
Australia
Finland
USSR
Chamois (Rupicapra rupicapra)
A zoonosis
Wombat, koala (Phascolarctos
cinereus) and fox (Vulpes vulpes)
Fox (Vulpes vulpes) and chamois
(Rupicapra rupicapra)
Fox (Vulpes vulpes)
Fox (Vulpes vulpes)
Fox (Vulpes vulpes)
A zoonosis
Isolated from wild animals; sporadic
cases among indigenous species
(marsupials)
Hares and wild birds
Rodents (rodent-sheep cycle)
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T A B L E I (contd.)
Disease name
Country which
provided
information
Salmonelloses
USA
Australia
France
Sweden
Wildlife species
and (when applicable)
susceptibility of man
A zoonosis
Small mammals and birds, infecting
poultry flocks
Isolated from wild animals; sporadic
cases among indigenous species
(marsupials)
Sparrows
Isolated from wild animals; only 3%
of foxes infected
A zoonosis
Erysipelothrix
infection
Australia
Isolated from wild animals; sporadic
cases among indigenous species
(marsupials)
Bulgaria
USSR
Rodents, birds and wild boar {Susscrofa)
Bulgaria
Losses among fallow deer (Dama
dama) and red deer (Cervus elaphus)
Verminous
gastro-enteritis
Bulgaria
Has reduced populations of red
deer (Cervus elaphus)
Porcine
parvovirus
infection
USSR
Enterotoxaemias
Wild boar (Sus scrofa)
SPECIFICITY OF INFECTIONS A N D INFESTATIONS
The specificity of infections and infestations is very well illustrated by the
herpesvirus infections in wild r u m i n a n t s , by Dictyocaulus spp. infestations in deer
and by the special case of infections a m o n g the wild fauna of Australia.
The specificity of herpesvirus infections in domestic and wild ruminants
Serological surveys have shown for some years (145) that numerous species of
wild animals possess specific antibodies which neutralise infectious bovine
rhinotracheitis (IBR) herpesvirus (Bovine herpesvirus 1). A list of such species is given
in Table II.
It has been found only recently that species other t h a n cattle can become infected
with a virus antigenically related to, but distinct from Bovine herpesvirus 1. A n initial
investigation (serological survey) suggested that other species can become infected
by the bovine virus, whereas subsequent and more thorough testing has demonstrated
718
t h a t they are, in fact, infected with a similar virus which is specific for t h e m . T h u s
goats were stated to be susceptible to IBR virus as a result of serological tests. In
fact, this species is most often infected by a herpesvirus of its own, Caprine
herpesvirus 2 (2, 44). Experimental infection of goats with Bovine herpesvirus 1
produces n o more than a mild infection, and the bovine virus fails to establish a latent
infection, indicating a lack of true adaptation (99).
A similar situation probably exists in the non-domesticated species which react
serologically t o Bovine herpesvirus 1. Three other herpesviruses related antigenically
T A B L E II
Range of susceptibility to infectious bovine rhinotracheitis
and antigenically related viruses
virus
Family
Subfamily
Species
Cervidae
Cervinae
Red deer (Cervus elaphus)
Eastern wapiti (Cervus canadensis)
Roe deer (Capreolus capreolus)
White-tailed deer (Odocoileus virginianus)
Mule deer (Odocoileus hemionus)
Elk (Alces alces)
Reindeer (Rangifer tarandus)
Caribou (Rangifer tarandus caribou)
Odocoilinae
Rangiferinae
Giraffidae
Giraffinae
Antilocapridae
Bovidae
Giraffe (Giraffa
camelopardalis)
Pronghorn (Antilocapra
Tragelaphinae
Bovinae
Alcelaphinae
Hippotraginae
Reduncinae
Antilopinae
Caprinae
americana)
Eland (Taurotragus oryx)
Greater kudu (Tragelaphus strepsiceros)
Domestic ox (Bos taurus)
Asian buffalo (Bubalus arnee)
African buffalo (Syncerus caffer)
Red hartebeest (Alcelaphus buselaphus)
Tsessebe (Damaliscus lunatus)
Blesbok (Damaliscus dorcas)
White-tailed gnu (Connochaetes gnou)
Brindled gnu (Connochaetes taurinus)
Roan antelope (Hippotragus equinus)
Sable antelope (Hippotragus niger)
Addax (Addax nasomaculatus)
Common Waterhuck (Kobus ellipsiprymnus)
Kob (Kobus kob)
Lechwe (Kobus leche)
Southern reedbuck (Redunca arundinum)
Bohar reedbuck (Redunca redunca)
Thomson's gazelle (Gazella thomsoni)
Springbok (Antidorcas marsupialis)
Tmpala (Aepyceros melampus)
Chamois (Rupicapra rupicapra)
Domestic goat (Capra aegagrus hircus)
719
to Bovine herpesvirus 1 have been isolated recently: type 1 herpesvirus of Cervidae
(55, 143), a herpesvirus of reindeer (Rangifer tarandus) (32, 33) and one of the Indian
buffalo (Bubalus arnee). T h e case of infection with cervid herpesvirus, isolated from
Cervus elaphus, provides a good example. Earlier serological surveys h a d revealed
antibodies specific for Bovine herpesvirus 1 in this species (63, 64), whereas recently
a herpesvirus of deer, antigenically related to the former virus, has been isolated (55)
from cases of conjunctivitis a m o n g fawns reared in Scotland. The frequency of this
infection varies according to particular circumstances, for the percentage of serological
conversions was 2 9 % in Great Britain (82) and only 1 1 % in Belgium (143, 145).
Specificity of the virus has been demonstrated (118), for deer could be infected with
their own virus, which remained latent after a primary infection, while infection with
the bovine virus failed (123). Conversely, when the bovine virus did multiply in deer,
the infection remained mild. T h e situation in deer is similar to that in goats, and
it is probable t h a t every case of serological conversion in deer is attributable t o the
cervid virus.
A remarkable finding is that, while the bovine virus can produce a moderate
infection in deer, the converse does not apply, and deer present n o risk for cattle.
Unfortunately, standard serological tests cannot distinguish the t w o types of
infection in deer, so they have been wrongly regarded as a potential source of infection
of cattle with Bovine herpesvirus 1.
M o r e precise techniques capable of distinguishing the two types of infection have
now become available (2), but they are difficult to apply.
A situation similar to that in deer m a y well exist in reindeer (Rangifer
tarandus).
Earlier serological surveys showed that 2 3 % of reindeer and a certain percentage of
caribous possessed antibodies to Bovine herpesvirus I (32, 34). A reindeer herpesvirus
has recently been isolated (33), t h o u g h experimental inoculation did not produce any
symptoms in reindeer. This virus proved, however, t o be pathogenic for cattle (84).
T h e situation in America is probably similar t o that in E u r o p e (22, 62). In Africa
it is rather m o r e complex, judging from the very high prevalence of antibodies t o
Bovine herpesvirus 1 observed in African buffalo (Syncerus caffer), eland (Taurotragus
oryx) and gnu (Connochaetes spp.) (47). Bovine herpesvirus 1 has been isolated from
gnu (59, 76, 75), t h o u g h the only lesion observed was that of vulvovaginitis. M a r é
(67) was unable to reproduce this disease in elands.
A p a r t from African buffalo (the susceptibility of which does not seem t o have
been elucidated), the gnu species is the only one k n o w n to be susceptible t o Bovine
herpesvirus 1. T h e infection remains confined to the genital tract, a n d it seems
improbable t h a t the infection would spread to other species, because of its sexual
transmission. Herpesviruses can persist latently in small populations of animals
without infection from outside (92, 88, 9 1 , 141). It therefore seems reasonable t o
assume t h a t other African species of wild ruminants, serologically positive to Bovine
herpesvirus 1, are infected with their own types of virus.
The problem of infection with bovine mammillitis herpesvirus (Bovine herpesvirus 2) is rather different. It is k n o w n that in cattle, from which the virus has been
isolated, the virus remains latent, and the infection is seldom manifested in the clinical
form (83).
720
In Africa, m a n y species have shown serological evidence of infection with this
virus (Table III) (104, 7 1 , 106, 41).
TABLE
III
Range of susceptibility to bovine mammillitis
or antigenically related viruses
herpesvirus
Family
Subfamily
Species
Giraffidae
Giraffinae
Giraffe (Giraffa
Bovidae
Tragelaphinae
Greater kudu (Tragelaphus strepsiceros)
Bushbuck (Tragelaphus scriptus)
Eland (Taurotragus oryx)
Domestic ox (Bos taurus)
African buffalo (Syncerus caffer)
Red hartebeest (Alcelaphus buselaphus)
Tsessebe (Damaliscus lunatus)
Brindled gnu (Connochaetes taurinus)
Roan antelope (Hippotragus equinus)
Sable antelope (Hippotragus niger)
Gemsbok (Oryx gazella)
Beisa oryx (Oryx beisa)
Common waterbuck (Kobus ellipsiprymnus)
Southern reedbuck (Redunca arundinum)
Defassa waterbuck (Kobus defassa)
Springbok (Antidorcas marsupialis)
Impala (Aepyceros melampus)
Domestic goat (Capra aegagrus hircus)
Domestic sheep (Ovis ammon aries)
Bovinae
Alcelaphinae
Hippotraginae
Reduncinae
Antilopinae
Caprinae
camelopardalis)
Although the virus has been isolated from African cattle (54) with a disease
resembling lumpy skin disease, it has not as yet been isolated from wild animals, with
the exception of the African buffalo (Syncerus caffer) (58, 106), which is particularly
close to the domesticated species.
Infection of wild species with Bovine herpesvirus 4 is not mentioned in the reports.
A n investigation in France and Belgium failed to find wild ruminants that were
serologically positive (144), although 2 2 % of Belgian cattle were positive.
Such a difference between domestic and wild animals is quite c o m m o n . F o r
example, in Belgium the percentage of wild animals serologically positive t o Bovine
herpesvirus 1 is very small (143) even t h o u g h it is a major pathogen of cattle. T h e
opposite situation occurs in Finland, where the infection is absent from cattle despite
positive tests in reindeer. This is another observation to confirm the rarity of transfer
of herpesvirus infections from wild species t o cattle, and vice versa, either because
of lack of contact between the two types of animals (particularly under conditions
of intensive husbandry) or for purely biological reasons, such as a specificity of the
infections and particular modes of transmission (e.g. sexual).
T h e special case of malignant catarrhal fever will be dealt with below.
721
The specificity of Dictyocaulus
infestations
A question is often raised concerning the threat posed by wild Cervidae as a
reservoir of Dictyocaulus species pathogenic for cattle.
A n investigation conducted recently in the United Kingdom (13) showed that fallow
deer (Dama dama) did not act as a reservoir of Dictyocaulus for cattle.
T h e possible role of red deer (Cervus elaphus) as a reservoir of bovine species
of Dictyocaulus has been questioned.
Studies of red deer reared for venison in the United Kingdom have shown t h a t
this deer harbours a Dictyocaulus sp. different from D. viviparus, which is responsible
for parasitic bronchitis in cattle (74), although n o difference is detectable between
the two species by the usual morphological examination. Consequently, deer are not
reservoirs of nematodes pathogenic for cattle.
Susceptibility of marsupials to infections of placental mammals
T h e Australian continent is a special and exceptional case.
Before the white m a n arrived, the only placental m a m m a l s on the continent were
h u m a n beings, dingoes (commensal with h u m a n beings), b a t s , rodents and coastal
aquatic m a m m a l s . T h e arrival of the white m a n coincided with the introduction of
numerous other species of placental m a m m a l s , some of which returned t o their wild
state: rabbit (Oryctolagus cuniculus), fox (Vulpes vulpes), water buffalo, cattle, pig,
dromedary, horse and donkey.
Although there is little information on the susceptibility of the indigenous mammals
to infections a n d infestations of introduced placental m a m m a l s , the report from
Australia clearly suggests that problems of cross-contamination (from wild or feral
species t o domesticated species) have arisen from the introduced domestic animals
that have returned t o the wild state.
This shows rather well that the phylogenic distance between eutherian m a m m a l s
and marsupials acts as a good barrier to cross-infection (existence of a refractory state).
The case of ornithosis-psittacosis (chlamydia infection)
This disease further illustrates the errors of interpretation which may arise from
a serological survey of wild or feral species. M a n y of the reports have emphasised
the risk posed by the feral pigeon (or rock dove, Columba livid) in transmitting
ornithosis to h u m a n beings.
Such statements are often based o n the results of serological testing, which show
a high proportion of serological conversions in these birds (38).
A n investigation in Belgium (151) has shown t h a t n o serologically positive pigeon
was excreting Chlamydia psittaci, confirming observations by Lüthgen in 1971 (66)
of a complete lack of agreement between the elimination of Chlamydia psittaci by
semi-domesticated pigeons and the titre of complement-fixing antibody in their serum.
This is confirmed by the absence of infection a m o n g pigeon fanciers, w h o constitute
the h u m a n population at greatest risk.
722
In fact, only psittacine birds pose a real threat. The reason for the discordance
in pigeons between the high percentage of serological conversion and the absence
of pathogen excretion may be explained by a different biology of the infection in
this species, since Chlamydia psittaci can be isolated from viscera (148).
RISKS TO W I L D A N I M A L S C R E A T E D BY D O M E S T I C A N I M A L S
The epidemiological links between domestic and wild species in the transmission
of certain diseases are often considered from a single direction only, a n d so there
m a y be a failure t o appreciate the risks to wild species posed by domestic species.
But this situation may also apply. T h e most striking example of infection of wild
species by domestic species is rinderpest, and one may also mention brucellosis and
tuberculosis.
Rinderpest
There can be no doubt that rinderpest is the most dangerous disease of cattle at
present (108). Of Asiatic origin, it has decimated E u r o p e a n herds during periods of
upheaval (such as wars). Complete eradication was achieved at the end of the last
century, apart from a brief reappearance in Belgium in 1920 (7, 90) and in the R o m e
Z o o in 1949 (24).
Until the last century, Egypt was the only African country to be infected
periodically. But in about 1880, on the occasion of the first Italian expedition to
Abyssinia, rinderpest spread along the Nile and thence to the entire African continent,
with the exception of N o r t h Africa, which is protected by the barrier of the Sahara
Desert (89). T h e history of rinderpest in Africa is therefore relatively recent.
T h e introduction of rinderpest by domestic cattle had severe effects o n big game.
As Table I shows, practically every species of the order Artiodactyla is probably
susceptible t o rinderpest virus, while the most susceptible species belong to the
Ruminantia and Suidae (102).
The wild animals originally infected by domestic animais were regarded for decades
as the reservoir of infection. They were invariably incriminated each time an outbreak
occurred among cattle. For this reason, control of the disease in East Africa (Tanzania
a n d Zambia) entailed the killing of m o r e t h a n 10,000 wild ruminants between 1941
and 1951. In fact, because certain wild species are very susceptible to this disease,
the appearance of rinderpest among wildlife may provide the first indication of the
presence of the disease in a given region.
In the past it was generally recognised that large concentrations of wild animals,
as in the Serengeti region of East Africa, could act as "long-term reservoirs" of the
virus, in the absence of the disease a m o n g cattle (111). This concept, still held by
some workers, is based essentially o n the discovery of specific antibodies in wild
animals (126). Even if this discovery is confirmed, it does not constitute sufficient
proof that wild species act as a reservoir of the virus (110).
In fact, a high frequency of antibodies in certain species m a y indicate merely t h a t
certain individuals of the species have become i m m u n e t o the disease (it is k n o w n
723
that cattle which survive the disease acquire a solid and durable immunity). T h e
question of specificity of the reactions was raised again recently, when antibodies
to rinderpest virus were detected a m o n g cattle in New Caledonia, where the disease
does not exist (Provost, personal communication).
F u r t h e r m o r e , there is a good argument against wild animals acting as a reservoir
of rinderpest. Elimination of the disease from cattle in South Africa following the
panzootic of 1888-1901 a n d in the Serengeti region of Tanzania between 1968 a n d
1970 was followed in each case by a diminution in the occurrence of neutralising
antibody in the wildlife population, which remained very dense in b o t h regions (108).
This seems t o suggest t h a t the disease m a y not occur among the wild animals of a
given region unless it is also occurring a m o n g domestic animals. Wild animals would
not therefore constitute a reservoir of rinderpest, and their role would be confined
to disseminating the disease by sporadic contact with domestic animals in an enzootic
or epizootic situation (107).
T h e question of the possible role of wild species in rinderpest is of major
importance, because it partly governs the success of the vaccination campaigns being
conducted at present o n African cattle (112).
Pest of small ruminants has never been reported a m o n g wild animals, although
an outbreak has been reported recently from a zoo at Al Ain, affecting representatives
of Gazellinae and Caprinae, also a member of Hippotraginae and possibly of
Tragelaphinae as well (37).
Brucellosis
Bovine brucellosis is another disease which has led to controversy about the possible
role of wild animals as a reservoir of infection. The problem arises mainly in European
countries trying to eradicate the disease. A serological survey in France showed that
only 2 of 54 red deer (Cervus elaphus) and none of 696 roe deer (Capreolus
capreolus)
possessed specific antibodies (12), so that wild Cervidae do not seem t o be involved
in the transmission of bovine brucellosis (69). It is probable that domestic animals
are responsible for infecting wild animals, and not vice versa, as demonstrated in
South Africa by the finding of brucellosis in African buffalo (Syncerus caffer) and
hippopotamus (Hippopotamus
amphibius).
In the same way, bison (Bison bison) and Cervidae have become infected in the USA.
Many European countries report the frequent occurrence of Brucella suis infection
among hares (Lepus capensis), following the observations of Witte (159), but without
being able t o establish an epidemiological link with the infection in pigs. As a
consequence of the intensive h u s b a n d r y of pigs, they have little possibility of contact
with hares.
Tuberculosis
There are numerous instances of inadvertent infection with mycobacteria,
particularly in species of wild animals kept in captivity in zoos, where they are exposed
to h u m a n infection. In South Africa tuberculosis has been diagnosed in m a n y wild
species, including African buffalo (Syncerus caffer), greater k u d u
(Tragelaphus
strepsiceros), c o m m o n duiker (Cephalophus (Sylvicapra) grimmia) and lechwe (Kobus
leche), from all of which Mycobacterium
bovis was isolated. These cases resulted
from wild animals coming into contact with h u m a n beings or domestic animals.
724
In Switzerland, M. bovis infection disappeared from game animals following its
eradication from cattle.
Roe deer (Capreolus
negative.
capreolus)
captured in France have all been serologically
A special situation apparently occurs in the United Kingdom, where the badger
(Meles meles) constitutes a wildlife reservoir of bovine tuberculosis (9). M. bovis has
been detected in 10% of badgers. In 1986, 4 3 % of the fresh outbreaks of tuberculosis
a m o n g cattle were attributed to infection from badgers (155, 156, 157).
This problem is particularly serious in South-West England, where badgers were
responsible for 6 5 % of outbreaks a m o n g cattle confirmed during 1986. There is a
high density of badgers in this region, in some places reaching 20 individuals per square
kilometre. Infected badgers excrete tubercle bacteria in their expectorations, faeces,
urine and in the pus of bite wounds. A p a r t from badgers, no other wild species seems
t o be involved in transmitting the disease to cattle. In regions where infected badgers
are found, there have been cases of tuberculosis in roe deer (Capreolus
capreolus)
a n d sika deer (Cervus nippon).
Red deer (Cervus elaphus) imported from
Czechoslovakia have also shown a high incidence of tuberculosis. The role of the
avian tubercle bacterium has yet to be established (27).
Because of the decisive role of badgers in transmitting tuberculosis t o cattle, the
authorities have taken steps to reduce the badger population in certain areas, and
are investigating an efficacious method of vaccinating them.
Conclusions
These examples show that the problem of epidemiological links between domestic
and wild animals must not be considered to occur just in one direction, and that certain
infections can disappear from wildlife when they are absent from domestic animals.
In some cases it m a y be better justified to protect wild species from contact with
domestic animals t h a n the reverse, particularly when the wild species are of economic
importance.
C U L T U R A L A N D ECONOMIC ROLE OF T H E F A U N A
The cultural and economic role of the fauna has changed considerably over the
last years in line with the way in which it is perceived by the general public, particularly
in developed countries. T o an increasing extent the fauna is regarded not as a
competitor t o the species reared by m a n , but as a complement, a resource to be
preserved, managed and developed (73, 129).
Long-standing attitudes regarding the use or destruction of wildlife resources must
now take into account the growing importance of environmental and conservational
viewpoints. T h e situation has changed in favour of rights for wild animals m o r e or
less comparable to those of domestic animals. In addition, in m a n y cases the wild
species have acquired an economic importance by involvement in recreation or as
a source of h u m a n food, and so they deserve to be treated in a way similar to domestic
animals.
725
Such changes in h u m a n attitudes to the larger wild animals have their influence
on the way in which epidemiological links between domestic and wild species are
perceived and m a n a g e d . They also affect the way in which the animals are managed.
Each change in cultural or food utilisation modifies the ecology of infections and
the host-parasite relationships, as well as possible relationships to domestic animals.
The situations which arise as a consequence can be classified as follows: national
parks and protected species; zoos and game parks; game ranches and farms; the rearing
of wild animals for repopulation.
National parks and protected species
In national parks the wild species are in an exceptionally favourable position, being
protected theoretically from the incursion of domestic species. The initial ecological
system is usually respected, and contacts with domestic species are practically nil.
In some cases there may be h u m a n intervention concerning the health status of certain
rare species. For example, in South Africa roan antelopes are systematically vaccinated
against a n t h r a x .
T h e situation m a y not always be as clear, however. T h e type of relationship
between domestic animals and big game, particularly in African countries, varies with
the type of land use (120).
L a n d m a y be used for grazing by domestic animals, or m a y form p a r t of game
reserves a n d national parks for use by the wild fauna. Because of the dominance of
transhumant husbandry in Africa it is obvious t h a t there is m o r e chance here t h a n
elsewhere of contact between domestic and wild animals.
Interrelationships a m o n g wild animals, domestic animals and the environment
may be summarised as follows:
a) On grazing
-
land:
competition for feed between wild a n d domestic animals;
- predation of domestic animals by wild carnivores;
-
erosion produced by the wildlife alone or in association with domestic stock;
- role of wild animals as reservoirs of diseases of domestic animals.
b) In the
-
reserves:
domestic animals may change the environment t o the detriment of wildlife;
- erosion produced by domestic animals alone or in association with the fauna,
to the detriment of the wild habitat;
-
domestic animals compete with wild animals for water a n d other needs.
Along with this list of unfavourable effects, it should be pointed out that
cohabitation between domestic and wild species may also have some beneficial effects,
provided that the proportions of the two groups are carefully regulated, a n d t h a t
they are complementary in feeding habits.
Zoos and game parks
These are also a quite special case because they unite within a n enclosed and
restricted area a collection varying in numbers and species, coming from very different
726
origins. The building up of a collection will draw on animals of unknown health status,
captured in their country of origin. As a consequence, zoos m a y provide ideal
conditions for the sharing of certain infections, and there have been some regrettably
spectacular incidents, such as the introduction of rinderpest into the R o m e Z o o in
1949, also the appearance of the African form of malignant catarrhal fever in a
European bison (Bos bonasus) in a Dutch zoo (139), and in the San Diego Zoo among
gaur (Bos gaurus), swamp deer (Cervus duvauceli) and banteng (Bos javanicus) (45).
There was likewise the recent and dramatic introduction of African horse sickness
into Spain by zebras from Namibia which were destined for safari parks (121). Because
of their isolation and special nature, however, zoos are only exceptionally a source
of infection to domestic stock in their vicinity.
Game ranches and farms
In many cases, wild species can provide a better renewable source of animal protein
t h a n domesticated species, particularly in Africa, where the natural ecological systems
are complex a n d often very fragile. Wild species m a y succeed better t h a n domestic
species in utilising the available plant resources, thereby enhancing productivity. Such
considerations have resulted in the establishment of ranches and farms for rearing
certain wild species.
This practice has developed considerably in certain African countries, such as
Z i m b a b w e . As a consequence, m a n y cattle farmers n o longer see game animals as
pests to be exterminated because they compete with domesticated species, but rather
as an important source of income. In ranching systems, cattle and game animals m a y
be reared together, apparently without creating any particular health problem. Some
breeders prefer to keep t h e m separate, with the wild animals inside enclosures to
prevent contact. By contrast, cattle m a y be kept within enclosures to protect t h e m
from contact with certain wild species such as the African buffalo, when this creates
a particular problem.
Such evolutions in husbandry practices should automatically engender new
approaches to health problems, including the study of the infections specific t o wild
species, and those shared with domesticated species. Another approach has been to
form herds of wild species exempt from certain infections, like the herds of African
buffalo (Syncerus caffer) in Zimbabwe which are exempt from foot and m o u t h disease.
Similar patterns may be seen in E u r o p e and New Zealand where deer farming,
particularly of red deer (Cervus elaphus) and fallow deer (Dama dama), has become
a n important activity. Red deer are reared o n a large scale in the United Kingdom,
particularly in Scotland, for venison. Deer have proved to be a better source of income
for the farmer t h a n sheep, the animal traditionally reared in the regions. The farming
of these species at high density has led to the emergence of new health problems which
must be investigated. Malignant catarrhal fever is the major cause of mortality beyond
a certain age (114, 143). Repeated contact with sheep is the main source of infection.
The existence of deer farms should lead to a reconsideration of the problem of
potential exchanges of infections with domesticated species, but once again in b o t h
directions.
Animals for repopulation
Certain species of game have become rare, particularly in E u r o p e , and this has
led to the creation of premises for repopulation, or the introduction of animals from
other countries better supplied with the species.
727
These practices have not always been accompanied by adequate disease control
precautions, particularly since the animals tolerate their t e m p o r a r y captivity very
poorly, and are therefore transported a n d released quickly.
Certain countries have thus complained that animals for repopulation have been
responsible for introducing disease into the indigenous fauna, with subsequent
transmission t o domestic animals. In Switzerland, for example, Brucella suis has been
found in hares introduced for repopulation.
It would clearly be desirable t o be m o r e vigilant a b o u t the health status of wild
animals reintroduced into a natural ecological system, for premises where the animals
are gathered together favour the exchange of infections between animals of the same
species.
Conclusion
The cultural and economic use of wild species creates new health problems, not
only with respect t o the possible infection of domestic animals, but also in regard
to the improvement of living conditions of wild species in their natural surroundings,
or under the conditions of some form of farming.
H E A L T H M A N A G E M E N T OF T H E WILD F A U N A
IN T H E N A T U R A L ENVIRONMENT
T h e new economic and cultural values attached t o wild species have altered the
conception of health problems as well as veterinary attitudes towards t h e m .
Whereas considerable progress has been m a d e in the control of diseases of
domesticated animals, there has not been nearly the same interest in infections and
infestations of wild species (128).
Particularly in Africa, veterinarians have incriminated wildlife as a source of
diseases of livestock, often without actual scientific proof. A widely held opinion
maintained that it was futile t o study wild species, because their diseases could be
overcome automatically by destroying t h e m or reducing their n u m b e r s . Because of
this attitude, m a n y research workers were prevented from conducting systematic and
well-organised research into the infections a n d infestations of wild species. Indeed,
such studies were often regarded as superfluous.
Some of these obstacles have n o w been lifted, and efforts are being m a d e t o
intervene and manage the health problems of wild animals, either to improve the
health of the animals or t o prevent possible transmission of a given disease to other
wild species, t o domestic animals, or t o m a n .
Examples of such intervention involve the treatment of parasitoses of Cervidae,
and vaccination of E u r o p e a n foxes against rabies.
Health management
T h e first problem raised by health management for wild species in their natural
surroundings is that of access t o the animals.
728
Under exceptional circumstances, such as the case of rare species in South African
national parks, individual animals m a y be handled in order t o vaccinate them against
a n t h r a x . In most cases, however, the preferred form of treatment is indirect. This
has long been the practice in E u r o p e for the control of the parasitic burden of deer,
which receive appropriate oral medication. Examples of such treatment have been
cited by Bulgaria.
Vaccinating foxes against rabies by the oral route
A notable example of preventive health intervention in the natural environment
is provided by the control of fox rabies in Europe. Contrary to the situation in regions
of Africa, America and Asia, the epidemiology of terrestrial rabies in E u r o p e is
relatively simple, for the red fox (Vulpes vulpes) is the principal reservoir and vector
(3). Attempts have been made t o vaccinate wild animals against rabies for more t h a n
twenty years (11).
The objectives of this prophylactic procedure are fundamentally the same as in
hygienic prophylaxis, except that instead of destroying the virus vector, the animals
are rendered refractory t o infection. Following a report by A n d r a l and Blancou (6),
the O I E is insisting o n guarantees that the procedure shall be innocuous for b o t h
target and non-target species.
The first criterion which any vaccination has t o comply with is efficacy.
Experiments conducted with attenuated strains of rabies virus have shown t h a t
strain S A D / B 1 9 , developed at the Tübingen Institute in Germany, is fully effective
in an adequate titre (16). The age of the animal at the time of vaccination is important,
for adult foxes respond better t h a n young ones.
The results of field trials of vaccination, conducted for the first time in Switzerland
(136, 137) and then in the Federal Republic of G e r m a n y (135) and other E u r o p e a n
countries (93, 36, 10, 18) have been very promising.
Between 65 and 7 5 % of foxes in a given region can be immunised by distributing
bait containing the vaccine. Other species which m a y compete with foxes in eating the
bait are badgers (Melesmeles), w i l d b o a r (Susscrofa) and certain small m a m m a l s (57).
A new way of vaccinating foxes against rabies by the oral route has been opened
u p with a vaccine containing recombinant vaccinia-rabies viruses, obtained by genetic
manipulation (61); Wiktor et al. (154) have already shown its efficacy.
This recombinant virus is perfectly efficacious and harmless for foxes, the target
species for vaccination in nature (17).
It is also safe for all non-target species tested so far, including badgers (Meies
meles) and wild boar (Sus scrofa), the principal competitors for taking bait (94).
Moreover, the recombinant virus is suitable for immunising young foxes (19).
T h e first field trial with recombinant virus vaccine was conducted in Belgium on
24 and 25 October 1987 (95).
T h e long-term consequences of vaccinating foxes against rabies have yet t o be
evaluated, for vaccination is giving rise to a novel situation in nature, that of a
population i m m u n e to a disease which formerly t o o k a practically inexorable course.
729
SOME SPECIAL CASES
Whereas the preceding chapters have concentrated on the general epidemiological
links between wildlife and domestic animals, the chapter which follows will describe
some special situations selected because of their importance, namely, malignant
catarrhal fever in Africa, African swine fever, foot and m o u t h disease in African
buffalo (Syncerus caffer), African horse sickness and pestivirus infections.
The African form of malignant catarrhal fever (MCF)
There are two forms of the disease, the African form associated with gnu and
caused by Alcelaphine herpesvirus 1 (AHV-1), and the E u r o p e a n form associated
with sheep, the virus of which has not yet been identified (although it is probably
a herpesvirus related t o AHV-1) (109).
The gnu-associated form is obviously encountered in Africa. Neutralising antibody
to A H V - 1 is c o m m o n l y found in members of the subfamily Alcelaphinae: the gnus
(Connochaetes taurinus and C. gnu), red hartebeest (Alcelaphus buselaphus), topi
or tsessebe (Damaliscus lunatus) and a member of the Hippotraginae, the beisa oryx
(Oryx beisa) (116, 113).
The virus has been isolated from gnu (100, 106),
been obtained from hartebeest a n d topi (78). T h e
pathogenic for cattle, because so far n o case of M C F
with topis, and inoculation of cattle with topi virus
a n d similar strains of virus have
topi virus does not seem t o be
has been associated with contact
does not reproduce the disease.
The mode of transmission between gnu and from gnu to cattle has been only partly
elucidated. Stress at the end of gestation and at calving may reactivate a latent infection
(130). In fact, a link between M C F in cattle and parturition in gnu has been k n o w n
for some time.
A fetal gnu m a y acquire infection within the uterus (101), although the virus has
not yet been demonstrated in fetal fluids and the placenta (127). Mushi et al. (77)
have suggested that the virus multiplies in gnu a n d is excreted in nasal and ocular
secretions (130) until 3-5 m o n t h s of age. Progressive development of active immunity
is probably responsible for the arrest of excretion (78).
Young, infected gnu can transmit the infection t o their contemporaries. By the
time they are one-year-old, most gnu have already been exposed t o infection. This
phenomenon is the origin of horizontal transmission of the virus between gnu a n d
from gnu t o cattle (79).
Although the virus can persist in gnu without provoking the disease, it is the incontact cattle that develop the typical form of M C F . A n d unlike the gnu, a bovine
is an epidemiological cul-de-sac, for there is n o transmission by contact with cattle.
This lack of transmission m a y be due to the occurrence of the virus inside cattle
in cell-associated form, whereas in gnu it is excreted in the free form. T h u s the virus
is well adapted to gnu, a n d infection of cattle is accidental.
These epidemiological features explain why, with the development of game farms
in South Africa, gnu-associated M C F has become the m a i n cause of mortality a m o n g
cattle resulting from contact with the fauna.
730
In cattle the disease occurs in March and April, 3-4 months after the calving season
of gnu, the delay corresponding to the incubation period. A n o t h e r peak occurs in
September-October and has yet to be explained.
The E u r o p e a n sheep-associated form of M C F is caused by a virus which has n o t
yet been fully identified (116). This form of the disease may coexist with the other
form in African countries which breed sheep, such as South Africa, and the two forms
cannot be distinguished clinically.
It is likely that cattle become infected by contact with infected sheep in a n
inapparent m a n n e r , although cases of M C F have been described in which there was
n o direct contact with sheep (68, 160).
The indirect immunofluorescence test with A H V - 1 antigen has revealed specific
antibodies in a high proportion of serum samples, even those from specific-pathogenfree lambs (SPF) (125). It is therefore probable that many viruses related antigenically
t o A H V - 1 occur in ruminants, particularly Caprinae, and are capable of producing
subclinical infections.
Whenever the virus passes the species barrier to infect cattle or deer, it becomes
pathogenic for these u n a d a p t e d , unnatural hosts (Reid, personal communication).
As mentioned above, deer are particularly susceptible t o M C F , the disease having
been first described in 1961 in a Père David deer (Elaphurus davidianus) (53); this
infection m a y have originated from gnu or sheep (115). Père David deer seem to be
the species most susceptible t o M C F (119). Cervidae are susceptible to b o t h sheepassociated and gnu-associated forms of the disease (134, 153, 114).
Whereas M C F occurs only sporadically among cattle, in deer it m a y occur in
epizootic form, involving a large number of animals. As early as 1906, Lupke described
the decimation of a herd of spotted deer (or chital, Axis axis) by a disease which
was probably M C F (114). A m o n g indigenous species, the disease has been described
in red deer (Cervus elaphus) of E u r o p e (114); also in the mule deer (Cervus hemionus)
(97) of N o r t h America a n d in white-tailed deer (Odocoileus virginianus) (160). In
Australia, New Zealand and the United Kingdom, where deer farming has become
an important part of the livestock industry, M C F is regarded as a major disease
problem. In cases which have occurred in New Zealand there has been n o contact
with sheep, and it has been suggested t h a t a deer/deer cycle m a y occur, or that a
reservoir host other t h a n sheep may exist (68).
African swine fever (ASF)
This disease is of considerable economic importance (132, 133). Morbidity and
mortality rates are very high, and m a y reach 100% during a primary infection. A t
present A S F occurs in an endemic state in many African countries south of the Sahara
a n d , outside Africa, in Spain, Portugal and Italy (Sardinia). Its area of distribution
is still expanding, and it makes brief incursions into territory outside its natural zone
of extension, such as Belgium (132, 14) and the Netherlands.
Domestic pigs (Sus scrofa domestica) and wild boar (Sus scrofa) are a m o n g the
species susceptible to A S F virus, and they are the only species to develop overt disease.
Wild African Suidae such as the warthog (Phacochoerus aethiopicus), bush pig
(Potamochoerus
porcus) and giant forest hog (Hylochoerus meinertzhageni)
are
equally susceptible, but the infection is inapparent, and these animals act solely as
731
asymptomatic carriers of the virus (51, 52, 103). Soft ticks of the genus Ornithodoros
are susceptible to the virus a n d constitute a reservoir and biological vector.
The area of distribution of wild Suidae in Africa, particularly warthogs, is extensive
south of the Sahara, and carriers of A S F virus have been detected in at least ten African
countries (158). T h e free-range rearing of pigs, extensive in intertropical Africa,
favours contacts between pigs and the natural reservoirs of the virus. In Africa there
is often a relationship between the presence of the disease in pigs and its presence
in wild Suidae, t h o u g h this is not invariably the case. F o r example, in South Africa
there is a relationship between wild Suidae possessing antibodies to the virus and the
occurrence of vector ticks (98), b u t in East Africa this does not always apply (105).
Warthogs infected when y o u n g seem t o remain carriers of the virus in their tissues
for a long time, probably for life, b u t only young animals develop viraemia with
excretion of virus (158). N o proof has been obtained so far of virus transmission
by contact between carrier warthogs a n d susceptible pigs (105).
While attempts to transmit A S F virus from wild Suidae t o pigs by simple contact
under experimental conditions have failed, it is well established that ticks can transmit
the virus when they feed o n pigs. Tick bites m a y be the origin of most primary
infections of pigs in Africa (103). There is also a cycle of virus transmission between
soft ticks (reservoir and vector) and warthogs (reservoir) during their period of
parturition. T h e existence of such a m o d e of virus conservation, independent of the
principal species affected (pig), m a y explain the appearance of A S F among pigs after
many years of absence.
Whereas adult wild African Suidae d o not excrete the virus and d o not transmit
it among themselves, the same does not apply to domestic pigs, for the virus has been
detected in excretions and secretions, a n d it is easy to produce direct transmission
from one individual t o another.
Taking into account the epidemiology of the disease, it should b e possible t o
prevent transmission of the disease from the wild reservoir to the domestic pig by
applying intensive husbandry methods coupled with strict observance of disease control
precautions.
Foot and moutb disease (FMD) in Africa
T h e list of species susceptible to F M D is very long, with most of t h e m belonging
to the Artiodactyla (49, 131), as shown by the list of susceptible African species
(Table IV). T h e most susceptible of African species is the African buffalo, Syncerus
caffer (20).
In order t o establish the role played by the fauna in the persistence and
dissemination of F M D , it is necessary t o find answers t o the following questions (5):
a) Which species are receptive t o the virus ?
b) D o these animals become ill and excrete a large quantity of virus ?
c) Which species become carriers of virus after a primary infection?
d) A r e wild animals carrying the virus capable of transmitting it to other animals,
particularly domestic animals ?
732
Almost 70 species of m a m m a l s belonging to m o r e t h a n 20 families are receptive
to natural or experimental infection with aphthovirus. There is considerable variation
a m o n g species in the degree of susceptibility. Whereas the African buffalo (Syncerus
caffer) and gnu rarely develop the clinical disease, greater k u d u
(Tragelaphus
strepsiceros), impala (Aepyceros melampus), warthog (Phacochoerus aethiopicus) and
bush pig (Potamochoerus
porcus) m a y develop severe clinical disease following
infection with aphthovirus (46).
Asymptomatic carriage of aphthovirus has been demonstrated in African buffalo
(Syncerus caffer) and greater k u d u (Tragelaphus
strepsiceros).
African buffalo can continue to carry the virus for more t h a n five years (25), a n d
the kudu for at least 140 days (46). Bovines which have recovered from the disease
can also carry the virus for long periods but, apart from these three groups, the other
species do not seem to become carriers. Thus the impala (Aepyceros melampus), which
is very susceptible to infection, does not carry the virus for long.
The question of transmission of aphthovirus by wild carriers to cattle remains
controversial.
C o n d y and Hedger (25) placed susceptible cattle into close contact with African
buffalo which were asymptomatic carriers for 2.5 years, during which time no cattle
became infected. This result is surprising in view of the ease with which contact
transmission normally occurs (29, 30). But the same authors have also obtained some
contradictory results (50). O n e m a y conclude t h a t the infection of cattle by wild
animals carrying the virus is a rare event. It does seem t h a t the African buffalo
(Syncerus caffer) and to a lesser extent the greater k u d u (Tragelaphus
strepsiceros)
play an important role in the persistence of aphthovirus in Africa within their o w n
populations, but without transferring it to domestic animals. The main characteristics
of the disease in buffalo are as follows (4): calves lose their passive immunity at 3-7
m o n t h s of age and then become susceptible to infection. T h e staggering of births
means t h a t there are always some individuals becoming susceptible. T h e source of
infection is either an adult carrier or an individual of the same age class with a primary
infection, excreting virus in amounts similar t o those excreted b y domestic cattle,
but for a longer period.
The result is that by three years of age, m o r e t h a n 8 0 % of buffalo will have been
exposed t o the three SAT types of the virus.
T h e present state of knowledge does n o t permit conclusions to be d r a w n o n the
role of wild species, particularly African buffalo, in the transmission of F M D to
domestic animals in Africa, particularly when the wide variability of strains is t a k e n
into account (20).
The role of the wild fauna, such as Cervidae in E u r o p e , seems to be even m o r e
limited (23).
A serological survey conducted recently in France (12) revealed o n e red deer
(Cervus elaphus) which possessed antibodies to type C aphthovirus. This finding was
not confirmed by subsequent investigations of deer of the same species, in which 77
samples were taken for virus isolation.
N o case of F M D was found in other members of the same deer population, nor
in domestic animals in the same area. T h e significance of such seroconversions thus
remains to be shown.
733
TABLE I V
receptive
Order/Family
Principal African species
to the virus of foot and mouth
(according to 49)
disease
Common name
Scientific name
Eland
Bushbuck
Greater kudu
African buffalo
Common duiker
Waterbuck
Reedbuck
Roan antelope
Sable antelope
Gemsbok
Tsessebe
Red hartebeest
Brindled gnu
Cape grysbok
Thomson's gazelle
Impala
Taurotragus spp.
Tragelaphus scrip tus
Tragelaphus strepsiceros
Syncerus caffer
Sylvicapra grimmia
Kobus ellipsiprymnus
Redunca arundinum
Hippotragus equinus
Hippotragus niger
Oryx gazella
Damaliscus lunatus
Alcelaphus buselaphus
Connochaetes taurinus
Raphicerus melanotis
Gazella thomsoni
Aepyceros melampus
Camelidae
Fallow deer
Giraffe
Bush pig
Warthog
Dromedary
Dama dama
Giraffa camelopardalis
Potamochoerus porcus
Phacochoerus aethiopicus
Camelus dromedarius
Insectívora
Erinaceidae
African hedgehog
Atelerix
Rodentia
Muridae
Rhizomyidae
Hystricidae
African rat
Mole rats
Porcupines
Arvicanthis abyssinicus
Terchyoryctes spp.
Hystrix galeata
Proboscidea
Elephantidae
African elephant
Loxodonta
Artiodactyla
Bovidae
Cervidae
Giraffidae
Suidae
albiventris
africana
In Switzerland wild boar became infected during an outbreak in 1960, while in
the USSR the saiga (Saiga tatarica) has been incriminated.
African horse sickness
This disease seems to have originated on the African continent, but did not become
recognised until susceptible animals were introduced from Europe into South Africa.
Only since then is there evidence of a primary reservoir a m o n g wild species.
734
Most of the zebras in South Africa possess specific antibody. Experimental
infection of zebras (35) results in a mild disease with a febrile attack, and occasionally
oedematous swelling of the hollow above the eyes. Viraemia lasts for 18 days. T h e
viraemic period may be important in the transmission of the virus by a r t h r o p o d
vectors.
T h e disease has made brief incursions into E u r o p e , particularly Spain (28, 121)
where the vector insects occur (72). T h e last incursion in 1987 probably resulted from
the introduction of zebras from Namibia.
Pestiviral infections
The recently defined pestivirus group comprises viruses of Artiodactyla having
close antigenic relationships (83). T h e three main pestiviruses isolated so far are
classical swine fever virus, bovine diarrhoea pestivirus ( B V D / M D virus) and border
disease virus of sheep. These viruses are pathogenic for their respective natural hosts,
and are capable of infecting other species (cross-infection). They possess the important
property of being able t o cross the placenta, producing congenital infection (150).
A disease resembling mucosal disease (MD) of cattle has been described in freeliving deer a n d a m o n g ruminants in a zoo, but without laboratory confirmation.
Similarly, cases of classical swine fever have been reported in wild b o a r , notably in
breeding premises for repopulation, a n d serological reactions t o classical swine fever
virus have been demonstrated in wild boar (15).
Pestiviruses have been isolated from roe deer (Capreolus capreolus) (122), red
deer (Cervus elaphus) (80) and fallow deer (Dama dama) (152) found dead, but the
contribution of virus to the disease is uncertain. Pestiviruses have also been obtained
from African buffalo (Syncerus caffer), giraffe (Giraffa camelopardalis)
and gnu
(Connochaetes spp.) (131).
Experimental infection of red deer (Cervus
conversion (70).
elaphus)
results in serological
Serological surveys have shown t h a t numerous species of ruminants in E u r o p e ,
North America and Africa (131) possess antibodies to BVD virus, but at low incidence
(64, 40, 60, 31). Thus a recent serological survey of red deer (Cervus elaphus) in the
United Kingdom revealed an incidence of only 5 % (Nettleton et al., unpublished
results), and the situation is similar in France (15).
T h e role of the wild fauna in the epidemiology of pestiviral infections remains
to be elucidated. In the present state of knowledge, wild species do not seem t o play
a determinant role in transmitting infection to domestic cattle. Here infection is
acquired essentially from immunotolerant cattle with persistent viraemia (81, 92).
CONCLUSIONS A N D
RECOMMENDATIONS
In order to establish the potential role of the wild fauna in the persistence and
dissemination of an infection shared with domestic animals, it is necessary t o answer
the questions posed by A n d e r s o n (5) in connection with foot and m o u t h disease:
a) Which species are susceptible t o infection?
735
b) Do these species develop clinical disease a n d do they excrete the causal agent
accordingly?
c) Which species become asymptomatic carriers after infection?
d) A r e the wildlife carriers capable of transmitting the disease t o other animals,
particularly domestic species ?
On the basis of these criteria, the diseases can be arranged roughly in three
categories:
1. Diseases having a k n o w n wildlife reservoir, such as rabies, African swine fever
and malignant catarrhal fever.
2. Diseases affecting m a n y domestic a n d / o r wild species but without a k n o w n
wildlife reservoir, such as rinderpest.
3. Diseases distributed equally between wild and domestic animals.
In the light of present information, it is often necessary t o reconsider our attitude
towards wildlife, which has been wrongly accused in the past of being the source of
most of the epizootic diseases affecting domestic animals.
O n the contrary, the history of rinderpest has shown that it m a y be necessary
to prevent contact between domestic a n d wild animals in order to protect the latter.
If wild animals are to be regarded as sources of protein and potential for recreation,
the problem must be viewed from two aspects: not only the risk incurred by domestic
animals in contact with wild animals, but also the risk incurred by wild animals in
contact with domestic animals. In addition, action may become necessary to improve
the health of the wild species, particularly in ecologically disturbed zones.
It must always be remembered that m a n y infections and infestations are strictly
specific and are not shared. T h e actual significance of the results of laboratory tests
often needs t o be re-examined.
One reason why epidemiological interactions between wild and domestic animals
have been little understood in the past is that studies have been made from the medical
perspective alone, ignoring the ecological factors which govern pathological
manifestations (128).
«
The economic and cultural status of wild species has undergone considerable
change in recent years.
In order to derive the most benefit from the economic and cultural development
of wildlife, it is vital t o improve our knowledge of the pathological aspects neglected
until now. Our knowledge is often fragmentary or inadequate. It should be set in
the context of a m o r e or less stable ecological system in which h u m a n beings also
participate.
A scheme for organising veterinary research for the rational use of wildlife was
proposed by Croze in 1981 (26). Application of such a scheme implies a readjustment
of thinking and a transformation of certain objectives currently pursued in veterinary
research.
Certain scientists, however, seem t o assume that the disease factor can be neglected
among wild species. This attitude is not justified by our existing knowledge (43).
736
Modification of natural ecological systems by bringing animals together in farms
leads to the appearance of new diseases, and upsets the host-parasite relationship.
In addition, there is often little or n o information a b o u t the
infestations of the wild fauna. Research needs t o be conducted on
including the specific infections of wildlife. Existing evidence of the
pathogens of domestic animals in wildlife is often indirect (serological
case requires verification by experimental inoculation to discover if
to be susceptible really are so.
infections and
m a n y subjects,
intervention of
evidence). Each
species reputed
Diagnostic tests need improved specificity, and they may have t o be adapted to
meet the actual situation. O u r epidemiological tools are, in fact, often unsuitable.
ACKNOWLEDGEMENTS
T h e authors are grateful t o Marinette Muys for preparing the typescript a n d to
M r A m a u r y Breuls de Tiecken for assistance in identifying the names of species. They
also wish to acknowledge assistance received from Dr L. Blajan, Director General
of the O I E , Georges Mees, Alex Donaldson and F i o n a Stuart. Useful criticism of
the manuscript was provided by Walter Plowright, Claude Louzis and Y. Ozawa.
T h a n k s are also extended to the translators.
*
* *
REFERENCES
(see p. 696)