Are domestic dogs the leading source of canine distemper in Serengeti carnivores? If this is the case, what are the possible routes of transmission? In which type of ecosystem are wild carnivores at most risk?
Eoin Kilkenny reg no. 1573/E
Canine Distemper Virus (CDV) is a single stranded RNA virus. Like measles
and Rinderpest, it belongs to the Genus Morbillovirus and the family Paramyxovirus.
Onset of the disease is rapid, with cytopathic effects evident just 12
to 10 days post infection (PI). Though there has been only one serotype
described for CDV, there are a variety of biotypes. i.e. though there
are strains of different genotype, there is no difference between the
distinguished set of antigens that are recognised by the immune systems
of potential hosts. These strains do however vary in their growth cycle
and their pathogenicity. Virulent CVD replicates best in B- or T-lymphocytes
or macrophages, thus weakening the hosts’ immune responses. Due to this
immunosuppression secondary infections may occur, with pneumonia, encephalitis
and hyperkeratosis of the footpads all commonly observed. After it has
invaded to lymphatic organs the virus then spreads to the surface epithelium
of the alimentary, respiratory and urogenital tracts. Infection can spread
through aerosol droplets, urine, faeces and ocular and nasal secretions.
Rates of transmission are thus extremely high for carnivores and especially
dogs who communicate via olfactory signals.
The virus can be spread to other individuals seven days post infection
(PI) and so an exposed and unprotected population in close contact with
each other are extremely vulnerable to CDV. The virus is also particularly
virulent with vulnerable individuals succumbing to the virus 2 to 4 weeks
post infection.
While CDV is most commonly associated with domestic dogs, there is a wide
range of susceptible hosts. Among the vulnerable families are Canidae,
Mephitidae, Mustelidae, Ailuridae, Hyaenidae, Procyonidae, Viverridae.
Also, while domestic cats are not in danger of infection, there have been
cases of infected lions (Panthera leo), tigers (Panthera tigris), and
leopards (Panthera pardus), both in captivity and in the wild.
From late 1993 to 1994 a CDV epidemic in the Serengeti ecosystem caused
a 30% decrease in the ion population. The areas affected were Serengeti
National Park, the Maswa Game Reserve in Tanzania and the Masai Mara National
Reserve, Kenya. The virus was isolated from the infected lions and the
antibody reaction patterns that it displayed were identical to those shown
by CDV strains isolated from domestic dogs. Virus isolates from hyaenas
and bat-eared foxes during the epidemic were also identical in this manner.
In fact, any variation in the virus strains across the Serengeti seemed
to be dependent on geographical location rather than host species. However,
while these studies showed that one strain of CDV was capable of infecting
both domestic dogs and wild carnivores, the routes of transmission between
and within species are still unresolved.
The International Union for Conservation of Nature (IUCN) has classed
the African lion as “vulnerable”. Already fragmented and isolated populations
of lions have lead to a higher probability of inbreeding and a decrease
in genetic heterozygosity and thus an inability to rapidly respond to
new environmental and pathological pressures. Clearly, the mal effects
of humans are complementing each other with regard to the strain they
are putting on the lion populations of the Serengeti.
Both Kenya and Tanzania extract a relatively large amount of their GDP
from ecotourism. The Masai Mara Game reserve attracts over 300,000 visitors
each year. The lion, being one of the “big five” (lion, leopard, buffalo,
elephant and rhinoceros), is a key species in attracting tourists and
big game hunters to the park. Worldwide lion numbers are estimated to
have dropped 30-50% in the past two decades. Should numbers continue to
drop, sightings would decrease due to smaller populations and increased
restrictions on hunting and even approaching this already declining species
would have to be implemented.
By attracting attention to the diversity and vulnerability of wild populations,
the lion and other large carnivores can act as ambassador species for
a specific ecosystem. Large animals, and especially carnivores, have been
used in the past to raise awareness of a ecosystem in distress, even if
they are not in fact the species most at risk. Thus, it is clear that
the lion populations are substantially valuable, both economically and
in terms conservation.
In this study, it was investigated whether the CDV epidemic that was recorded
in the lion population of the Serengeti could in fact be sourced to domestic
dogs. The dog populations were serologically examined (a seropositive
individual has had an immune response to a CDV infection whereas a seronegative
individual has not) Specifically, areas of high and low density domestic
dog populations adjacent to the park were used to analyse (i) CDV age-seroprevalence
patterns (ii) disease-related mortality and (iii) survival of CDV seropositives
and seronegatives.
Methods
For the Ngorongoro district, inhabited primarily by Maasai people, human
population was estimated based on a previous census and projected population
growth. Estimates of dog densities was then predicted from these data
and was found to range from 0.38 to 0.46 dogs/km2 from 1992 to 1994. Dog
densities for the serengeti district were estimated in the same manner
and were found to be higher than those of the Ngorongoro district, ranging
from 5.72 to 7.17 dogs/km2.
Data were collected for three periods: September 1992 to February 1993;
September to December 1993; August to December 1994. Questionnaires were
distributed to one in every five households along a transect in order
to collect demographic data on the dogs. These data consisted of age,
sex, and clinical history. If a dog had died during the course of the
study the month of death and suspected cause of mortality was also noted.
Blood samples were also taken from these dogs. Blood samples from previous
rabies vaccination trials were also used. Serum antibody tests were then
carried out and categorized according to age, year and area of origin.
The effect of age, region and and year on mortality was then investigtated
by carrying out a regression analysis for seropositivity and cause of
death.
Results
A dilution threshold for antibody titres was used as a cut off point to
distinguish between seropositive and seronegative individuals. For analysis
of age-seroprevalence data, three age categories were established: 0-1
years 1-2 years and >2 years. In both the Serengetti district and the
Ngorongoro district, there was a higher proportion of seropositives in
the higher age classes. Controlling for age, there was a significant difference
in seroprevalence between years in the Ngorongoro district but not in
the Serengeti district. There were significantly more seropositive pups
recorded in 1994.
While overall annual mortality was similar in the two districts, disease
related mortality was influenced by geographical area and year. Disease
associated mortality was significantly different between years for Ngorongoro
but not Serengeti.
The survival rate of seropositives versus seronegatives was then carried
out for both districts. It was found that in the Serengeti district, there
was no significant difference between the suvival rates of CDV seropositives
and seronegatives. However, in the Ngorongoro district there was a higher
mortality rate for seronegatives rather than seropositives. This difference
was significantly greater for the period 1993-1994 than for 1992-1993.
Discussion
The significant differences in age-dependent seroprevalence patterns from
year to year in the Ngorongoro district suggests that a low density dog
population cannot sustain the virus between outbreaks. The patterns indicate
that there was an outbreak in 1991, and that the seronegative pups born
in 1992 and 1993 were not exposed to infection. Seropositive pups observed
in 1994, however, suggest that the virus had again been introduced to
the population. These interpretaions are consistant with clinical observations
of the domestic dog populations during these periods. Seropositive pups
were, however, present in all years of the study in the Serengeti district.
It seems that that the higher density population allows the virus to persist
from year to year.
The owner questionnaires were unlikely to provide a solid basis for any
scientific argument on CDV epidemics and they were not used for any statistical
analysis in this study. The survival rates of seronegative and serpositive
individuals could however be interpreted by examining the surviving pups.
In 1994, the Ngorongoro population experienced a higher rate of seronegative
mortality than in previous years. In contrast, the mortality of seronegatives
remained relativley constant throughout the study in the Serengeti population.
This again supports a more consistant rate of infection in a higher density
population form year to year.
Regarding the CDV epidemic in the Serengeti lion population, there are
three realistic hypotheses as to how the virus was introduced. The first
is via the Ngorongoro domestic dog population. This is an unlikely source
however because when this population was exposed in late 1994, as the
seropositive pups suggested, infection was already spreading south through
the lion population. In contrast, the Serengeti dog population was exposed
the virus throughout the years and was thus a possible source of the CDV
transmission. The third possibility was that domestic dogs were not the
source and that CDV had been maintained in wildlife reservoirs until it
struck the lion populations. While there are numerous species that could
have maintained the virus for spaces of time, there is no direct evidence
to suggest that this is the case. Also, if low density dog populations
are unable to sustain the virus then it is unlikely that wild populations
could occur at sufficient densities for pathogen sustainability. Finally,
studies of CDV epidemics in lion populations and also in hyaenas suggest
that rather than persistant exposure to infection, the outbreaks have
been sporadic. Mortality rates also indicate populations that were not
accustomed to infection.
If the domestic dogs are indded the source of CDV infecting the Serengeti
wildlife then the question remains, what are the routes of transmission?
A number of factors come into play when trying to map these routes, including
the community structure of the host(s), population density and therefore
contact rates, pathogen virulence, and anthropogenic and biogeographical
factors, all of which may be influenced by eachother. Domestic dogs are
social animals and intraspecific transmission is clearly possible at sufficient
densities. However, they may also come into contact with wildlife. Low
ranking male hyaenas are often driven away from kills and forced to scavange
in villages. This hypothesis is supported by the fact that low ranking
males had a higher seropositivity than high ranking individuals. Lions
are also extremely social and feed together, facilitating transmission
to their own species and also any other carnivores that may be present
at that kill afterward. Predators will follow their prey so a decrease
in prey density or a clustered distribution will increase contact between
predaotrs. Domestic dogs will also be attracted to carcasses and may then
come into contact with wild carnivores either directly or via a common
feeding site.
Once the infection manifests itself in the wild it is then a question
of whether it can establish itself and persist. A low density host population
is more vulnerable to a pathogen with low virulence as high virulence
would simply kill off the infected fast enough to prevent transmission.
However CDV has high virulence and as seen in the domestic dogs, it does
not thrive in low density populations. This is reflected in wild populations
also. In 1996 there was an epidemic that resulted in the disappearance
of 5 packs of wild dogs from south african parks. In these instances,
the outbreaks were confined to populations in the high density flood plains
but not to the low density mopane woodlands. In these cases it is often
ecotone structure limiting population size either directly or by influencing
prey distribution. High landscape heterogeneity can result in population
density changes and if the density drops below the critical point for
a particular pathogen it will not persist. In east Africa, the landscape
is generally more homogenous than in southern and west Africa. Therefore,
contact between communities of carnivores is much more common in the east
and has experienced widespread mortality from pathogens such as CDV.
As the human population continues to expand contact with domestic and
wild animals is certain to increase. Vaccination of domestic dogs against
diseases such as CDV and rabies is therefore essential to the maintennance
of healthy populations of wild carnivores. As it is not always possible
to vaccinate every domestic animal, factors such as those described here
should be taken into account when assessing populations that are the biggest
threat to the wildlife surrounding them. It seems that areas of high domestic
dog sensity in close contact with wild carnivores on homogenous landscapes
are at a high risk of spreading disease. Also, anthropogenic factors such
as hunting will both reduce prey numbers increasing predator-predator
contact and also attract carnivores to kills. If activities such as big
game-hunting were to be organised in areas of low risk then perhaps levels
of transmission could be minimized.
References
Alexander KA, McNutt JW, Briggs MB, Standers PE, Funston P, Hemson G,
Keet D, Van Vuuren M. (2008) Multi-host pathogens and carnivore management
in southern Africa. CIMID 10.1016
Cleaveland S, Appel MG, Chalmers WS, Chillingworth C, Kaare M, Dye C.
(2000) Serological and demographic evidence for domestic dogs as a source
of canine distemper virus infection for Serengeti wildlife. Vet Microbiol
2000;72:217-27.
Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, et al. (1996) A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 1996;379:441-5.