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Donovan Tokuyama

Prof. William Durham & Dr. Susan Charnley

ANTHRO 12SC

15 October 2017

Who Let the Dogs Out?: Causes of canine distemper in East African wildlife populations and

possible mitigation strategies

ABSTRACT

Carnivores in Tanzania’s famed Serengeti and Ngorongoro ecosystems are being

increasingly affected by the spread of canine distemper virus. The virus has displayed the ability

to mutate at a rapid rate, thereby evolving into strains adapted to hosts outside the historical range.

This growing and expanding host range has led to the maintenance of the virus in wildlife

populations, as opposed to the more obvious domestic dog reservoir. As a result, the validity of

efforts to limit the spread of canine distemper virus through domestic dog vaccination campaigns

has been called into question, as have the circumstances leading to outbreaks of the virus. This

paper will investigate the role of genetics in specific outbreaks, how other environmental factors

influence an outbreak, and the merits of the vaccination campaign in the fight against canine

distemper.

INTRODUCTION

i. Canine Distemper Virus

Canine distemper virus (CDV) is a highly infectious morbillivirus present on all seven

continents, in part due to an ever-growing list of potential hosts. CDV, as with other

morbilliviruses like rinderpest, is characterized by its severe pathogenicity (Beineke et al 2015).

Transmission of CDV occurs primarily through respiration, either due to the viral shedding of

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other animals or through direct contact with infected

organisms. Most of the secretions and excretions of infected

animals facilitate the shedding of CDV; however, as the

virus is unable to survive for more than a few hours outside

of a host, the majority of disease transmission occurs

through contact between organisms. Once an organism

clears the virus it is considered to be immune to future

infections; therefore, young and/or immunologically

susceptible organisms hold the highest risk for infection

(Miller et al 2009). This characteristic additionally results in the young acting as a reservoir for

the disease.

Clinical symptoms of CDV do not appear in every case of viral contraction; current

estimates place the probability of symptoms arising in dogs lie between twenty-five and seventy-

five percent. However, when symptoms are shown, the disease has a high mortality rate – estimated

at around fifty percent of cases (Miller et al 2009). Additionally, CDV causes a systemic infection

of almost all organ systems, including respiratory, digestive, and nervous (Beineke et al 2015).

Infected dogs, for example, first become febrile before exhibiting symptoms such as ocular and

nasal discharge, conjunctivitis, and weight loss. In some cases, extensive neurological damage

may occur, resulting in petite mal and grand mal seizures (Miller et al 2009).

Perhaps deadlier than the virus itself, though, are the coinfections arising from CDV-

related immunosuppression. CDV is propagated through the lymphatic system; more specifically,

the T- and B-lymphocytes, responsible for recognizing pathogens, serve as the sites for viral

replication (Miller et al 2009). This depletion of lymphocytes in the blood in turn prevents the

Figure 1A: Artistic rendition

of the canine distemper virus.

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immune system from functioning properly. An organism with an inhibited immune system is much

more susceptible to disease; CDV-infected organisms often contract bacterial infections like

pneumonia and parasite-related illnesses like babesiosis (Munson et al 2008). If it is not the CDV

that proves fatal, then it is commonly these aforementioned coinfections that do.

ii. CDV in the Serengeti-Ngorongoro Ecosystem

CDV’s origins in the Serengeti-Ngorongoro ecosystem have historically been attributed to

the presence of a domestic dog population in the region (Roelke-Parker et al 1996). Recent

estimates place the size of this population somewhere between 30,000 and 50,000 dogs (Viana et

al 2015). As a result, the significant pup population serves as the primary reservoir through which

CDV is propagated and maintained (Roelke-Parker et al 1996). Additionally, disease spillover

Figure 1B: (clockwise, from top left) Bat-eared fox (Otocyon megalotis), the African wild dog

(Lycaon pictus), the African lion (Panthera leo), and the spotted hyena (Crocuta crocuta).

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from domestic dogs into wildlife populations has increased as human-animal contact and conflict

has increased. Canidae organisms in the Serengeti-Ngorongoro ecosystem (Figure 1B) include the

African wild dog (Lycaon pictus) and the bat-eared fox (Otocyon megalotis). However, it has been

hypothesized that disease outbreaks in wildlife populations may not be solely caused by

interactions with domestic dogs as there is evidence supporting the claim that CDV can be

maintained in wildlife reservoirs (Nikolin et al 2017).

A cause for greater concern, though, is that CDV has become increasingly common in

organisms outside of its typical host range (Martinez-Gutierrez et al 2016). A 2016 data

agglomeration by Marlen Martinez-Gutierrez and Julian Rey-Saenz of Universidad Cooperativa

de Colombia found that upwards of one hundred species from five different orders (including

Canidae) have shown to be susceptible to CDV infection (Figure 1C). With regards to the

Serengeti-Ngorongoro region (Figure 1B), lions (Panthera leo) and spotted hyenas (Crocuta

crocuta) have been most heavily affected by this expanding host range (Carpenter et al 1998). A

2001 epidemic in the Ngorongoro Crater resulted in the death or disappearance of twenty-four of

the crater’s sixty-one total lions over the course of ten weeks (Munson et al 2008). This dramatic

reduction in numbers illustrates the magnitude of northern Tanzania’s CDV problem. Top-down

Order # of Families # of Species

Carnivora 12 96

Rodentia 4 4

Primates 2 4

Artiodactyla 3 4

Proboscidea 1 1

Figure 1C: Chart illustrating the diversity in animals affected by CDV.

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regulation of the ecosystem’s apex predators has wide ranging implications for the ecosystem as a

whole: increased herbivore populations, increased grassland degradation, and so on.

HYPOTHESES

i. Lions living within the Ngorongoro Crater are particularly susceptible to CDV epidemics

due to a population bottleneck.

ii. Environmental factors play a major role in determining the potency of a CDV lion epidemic.

iii. One effective method for preventing CDV exposure and epidemics is the vaccination

campaign.

RESULTS & DISCUSSION

i. Hypothesis 1: Population Bottleneck

The Ngorongoro Crater is a 250 kilometer-squared collapsed volcanic crater located in the

southeast of the Ngorongoro Conservation Area in northern Tanzania. The crater is home to a

diverse and significant population of wildlife, making it a popular destination for tourists and

scientists alike (Packer et al 1991). Within the crater exists a well-studied population of lions, for

which population, serological, and genetic data is available going back to as early as the 1960s.

For this reason, the Ngorongoro crater lions serve as an ideal study population.

Population data has indicated that the Ngorongoro Crater has an upper carrying capacity

of around one hundred to one hundred and twenty lions. However, since the 1990’s, the population

of lions in the crater has been fairly volatile; the population has oscillated rapidly between sixty to

seventy lions and thirty to forty lions (Kissui et al 2004) (Figure 2A). Research conducted by

Bernard Kissui and Craig Packer from the University of Minnesota found that neither prey

availability or interspecies competition (i.e. hyenas stealing a lion kill) were decisive factors in the

decline and subsequent population instability. Rather, they identified disease as the primary factor

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Figure 2A: Ngorongoro Crater lion population data from 1962 to 2002. Dotted line

represents total population. (Kissui et al 2004)

Figure 2B: Ngorongoro Crater lion population data, emphasizing the dramatic drop in 1962.

(Packer et al 1991)

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for the population dynamics observed. They further note that the lions within Ngorongoro Crater

have an even greater risk of contracting illnesses such as canine distemper because of significant

inbreeding within the crater population (Kissui et al 2004).

Following heavy rains and a dramatic increase in the numbers of disease-carrying Stomoxys

calcitrans flies, the population of lions in the Ngorongoro Crater crashed; the population fell from

an estimated seventy-five lions to just ten (Figure 2B) (Packer et al 1991). The implications of this

severe reduction in numbers was that a handful of lions were responsible for the subsequent

repopulation of the crater. Coupled with a low amount of gene flow into the crater, the population

has become significantly inbred over time: when compared to lions just west in the Serengeti, the

lions in Ngorongoro displayed lower amount of genetic diversity (Figure 2C) (Packer et al 1991).

With this inbreeding comes the ramifications of reduced diversity; the lions in Ngorongoro Crater

find themselves at an increased risk of potentially devastating disease epidemics.

Considering the effects of decades of inbreeding within the crater as well as the influence

of disease on the crater’s population, there is justification for identifying a correlation between the

two. Clearly, lions in the crater are dying in significant numbers from disease (more specifically,

Figure 2C: Data contrasting genetic diversity levels in the Serengeti with levels in

Ngorongoro. Allele frequencies indicate more genetic similarity in Ngorongoro. (Packer et al

1991)

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from CDV or CDV-related coinfections) and these lions also suffer from the effects of genetic

homogeneity. It is important, though, to make the distinction that the Ngorongoro lions are not any

more likely to be exposed to or to contract CDV than any other geographically distinct counterpart.

It is simply that these lions are more likely to experience a significant epidemic due to the lack of

genetic diversity. The 2001 epidemic was the only major outbreak in recent history, and, while

homozygosity certainly influenced the outcome of this outbreak, it was not caused solely by this

(Munson et al 2008). There are many other factors that influence CDV outbreaks, as will be

detailed later in this paper.

ii. Hypothesis 2: Environmental Factors

It has been shown that the exposure of a population to CDV does not always result in an

outbreak of distemper (Figure 3A) (Viana et al 2015). Dubbed “silent epidemics,” these periods of

CDV seroprevalence that do not result in lions exhibiting clinical symptom indicate that

transmission alone does not cause outbreaks (Munson et al 2008). Environmental data highlight

specific circumstances preceding both the 1994 Serengeti outbreak and the 2001 Ngorongoro

outbreak that were not factors in the silent epidemics. More specifically, outbreaks typically

followed a period of severe drought, after which heavy rains promoted the explosive growth of

disease-carrying insect populations. Additionally, there is evidence supporting the notion that

human-related environmental manipulation helped to create conditions conducive to the spread of

CDV (Munson et al 2008).

The University of California, Davis’ Linda Munson identified several factors that

influenced the outbreak of CDV that occurred in the Serengeti in 1994. The aforementioned pattern

of severe drought followed by heavy rainfall can be seeing in Figure 3B (Mduma et al 1999).

Concurrently with the drought, the amount of food available per animal in the region dropped

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dramatically, leading to weakened and reduced herbivore populations. These animals became easy

prey for ticks, resulting in an explosive growth in the tick population. Additionally, the lack of

proper nutrition made it more difficult for animals like the Cape buffalo (Syncerus caffer) to fight

Figure 3A: Evidence of “silent outbreaks” in the Serengeti and Ngorongoro Crater. Grey

bars indicate increased CDV seroprevalence without manifestation of clinical symptoms

while red bars indicate the timing of actual outbreaks. Black lines represent population.

(Munson et al 2008)

Figure 3B: Environmental data showing dramatic reduction in rainfall and food levels just

prior to the 1994 Serengeti outbreak. (Mduma et al 1999)

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off tick-transmitted diseases like babesiosis. Upon ingesting the diseased meat of these animals,

Serengeti lions also contracted the Babesia haemoparasite. Data reveals a strong correlation

between high rates of babesiosis and mortality, suggesting that coinfection was a major cause of

the death of lions in 1994 (Figure 3C).

Munson does note, though, that lions in these silent epidemics also faced infection by

Babesia and were similarly immunosuppressed. The distinguishing factors was the severity of the

Babesia outbreak, which was heavily influence by the environmental factors leading up to the

epidemic (Munson et al 2008).

Similarly, the 2001 Ngorongoro Crater epidemic can be attributed in part to the

proliferation of ticks in the grassland ecosystem. However, this proliferation came as a result of a

restriction of burning within the crater following the expulsion of Maasai settlements from the

Figure 3C: Data showing a positive correlation between increased levels of babesiosis and

mortality rates. Serengeti prides are represented by blue triangles and Ngorongoro prides by

red circles. (Munson et al 2008)

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crater floor in 1974. Historically, the Maasai’s controlled burning of the grazing land kept the grass

from growing out of control: taller, coarser grass would be burnt such that shorter grass could grow.

This rangeland management not only served the Maasai’s pastoral interests, but also fostered a

diverse herbivore community (Fyumagwa et al 2007).

Following the prescribed burning ban within the crater, the grassland composition began

to change. The aforementioned taller, coarser grass became dominant and, with this, came animals

favoring this type of vegetation such as the Cape buffalo. With the grass providing protection from

UV light and with the presence of preferred hosts, tick numbers increased dramatically (Figure

3D). Ultimately, this proliferation of ticks played a role in the deadliness of the 2001 epidemic

(Fyumagwa et al 2007). The 2001 epidemic brought attention to the burgeoning tick numbers and

controlled burning was reinstated shortly after (Figure 3F). Almost immediately, tick numbers

were dramatically reduced. Peak numbers fell from almost 1000 ticks per square meter prior to

2001 to less than 600 after (Figure 3E). Corresponding with this reduction in tick numbers was a

reduction in tick-borne disease prevalence (Fyumagwa et al 2007).

Figure 3D (left): Tick numbers prior to the reinstatement of controlled burns.

Figure 3E (right): Tick numbers following the reinstatement of controlled burns. (Fyumagwa

et al 2007).

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The data regarding environmental factors prior to the 1994 and 2001 outbreaks,

respectively, seem to clearly indicate that these various other elements play a major role in

determining whether or not exposure becomes an epidemic. A recent genetic characterization study

of the disease, however, indicates that the strain of the virus must be adapted to the host species

before these environmental factors can play a role (Nikolin et al 2017).

Phylogenetic testing of various CDV strains revealed that strains can be distinguished at a

molecular level: certain strains appear to be well-adapted for cellular environments in non-canids

Figure 3G: Base pair comparison of four strains of CDV against a 2007 strain. 1994 strains

show higher levels of similarity as well as distinction between canid/non-canid strains.

(Nikolin et al 2017).

Figure 3F (left): Phylogenetic relationship between 1994 CDV strains.

Figure 3H (right): Controlled burn area in the Ngorongoro Crater.

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while others are more suitable for canids (Figure 3G). For example, in the case of the 1994

outbreak, the strains can all be traced back to a virus found in a US domestic dog. However,

subsequent mutations resulted in two separate lineages forming: one of a canid adapted strain that

afflicted Serengeti domestic dog and a non-canid adapted strain that afflicted lions and hyenas

(Figure 3H). As a result, it the case where a family is infected by a strain adapted to another family,

these organisms can more easily clear the virus. Silent epidemics can thus be attributed to exposure

to non-adapted strains, while epidemics are a combination of exposure to adapted strains and

environmental cofactors (Nikolin et al 2017).

iii. Hypothesis 3: Vaccination

The substantial domestic dog population surrounding and permeating the Serengeti-

Ngorongoro ecosystem has often been cited as the primary reservoir for CDV and, thus, the

primary vector by which CDV is transmitted to wildlife (Figure 4A) (Cleaveland et al 2000).

Indeed, with a population estimated to be in the tens of thousands, domestic dogs have historically

maintained the disease and facilitated transmission (Kapil et al 2011). Further, these populations

are characterized and being endemically infected with the virus (van de Bildt et al 2002). Prior to

1994, infection peaks in dog preceded infection peaks in lions, suggesting that disease spillover

was driven by domestic dogs (Figure 4B) (Viana et al 2015). As a result, many have traditionally

called for the use of widespread vaccination campaigns to, if not eliminate, dramatically reduce

the prevalence of CDV (Di Sabatino et al 2015). Indeed, campaigns against CDV have had success

in the past: a campaign in Finland in the 1990’s virtually eliminated the disease in the domestic

dog population (Rikula et al 2007).

However, the frequency mutation rate and rapidly expanding host range have changed the

mechanisms by which CDV operates in northern Tanzania. An emerging trend of asynchronicity

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between lion and dog CDV exposure indicates that modes of transmission are changing; essentially,

that domestic dog are no longer the only population transmitting CDV to lions (Figure 4B) (Viana

Figure 4A: Domestic dogs in the Serengeti-Ngorongoro ecosystem.

Figure 4B: Data comparing peaks of dog infection and lion infection. Data becomes less

synchronous following 1994, indicating a change in the methods of transmission. (Viana et al

2015)

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et al 2015). Other wildlife populations, such as wild dogs, jackals, and hyenas, have now been

identified as being viral reservoirs for CDV (Beineke et al 2015, Goller et al 2010). Additionally,

the employment of government-sponsored vaccination campaigns in the region have shown to be

effective in curtailing domestic dog contraction; however, the continuing prevalence of the virus

in lions and other wildlife indicate that the success is not ubiquitous (Viana et al 2015).

While domestic dog-centric vaccination campaigns have not stopped the transmission of

the virus to wildlife populations, it is important to make the distinction that the intensity of

seroprevalence peaks have declined. That is to say, the vaccination of domestic dogs is having an

effect; however, this effect is not substantial enough to warrant the effort a success in terms of

wildlife protection (Figure 4C) (Viana et al 2015).

Citing these trends, some have argued for the employment of wildlife vaccination

campaigns to reduce CDV. Many game wardens, though, are still wary of utilizing these due to an

attempted vaccination effort in African wild dogs. In this study, a litter of pups were vaccinated

against CDV and subsequently all died and their deaths were attributed to vaccine-related CDV

infections (Durchfeld et al 1990). However, this theory has been widely debunked and wildlife

vaccines have been proven safe (Viana et al 2015).

Figure 4C: Data

showing a decrease

in CDV

seroprevalence and

asynchronous

infection peaks.

(Viana et al 2015)

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CONCLUSION

The dynamics of canine distemper virus are complex and evolving. In an area where there

are an estimated 30,000 to 50,000 domestic dogs and upward of 3,000 lions, understanding CDV

is of paramount importance (Riggio et al 2012). Clearly, there are many factors that are at play

when a CDV epidemic occurs. From hypothesis one, the genetic makeup of a population may

predispose them to devastating outbreaks. From hypothesis two, not only environmental factors

like rainfall, but also human influence can determine whether exposure turns into an outbreak or

not. Additionally, CDV strains are distinguished by their adaptations: some strains are adapted for

canid hosts while others are not. These adaptations play a major role in determine the outcome of

exposure. From hypothesis three, vaccination campaigns do work in curtailing CDV; however, it

depends on the population these campaigns are trying to protect. With regards to lions, domestic

dog vaccinations have not proven effective as the mutation of the disease has created wildlife

reservoirs through which CDV can be spread.

It is important to continue investigating the dynamics and forces at play in canine distemper

outbreaks. As Tanzania boasts one of the world’s largest remaining lion populations, it is of great

importance to do further research into effective curtailment/mitigation strategies, disease detection

methods, and treatment options.

ACKNOWLEDGEMENTS

To the Sophomore College program for creating a space where experiences like this are possible;

to Stanford Travel/Study for making this trip a reality; to all of the hotel staff who made every

effort to ensure our comfort and enjoyment; to our wonderful Hoopoe guides for imparting upon

us their boundless knowledge and experience; to the outstanding alumni, who’s eagerness to learn

and kindheartedness inspired, motivated, and excited me; to my irreplaceable peers, who taught

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me to be a better person, with who I laughed and cried, and for whom I am eternally thankful; to

our SCA’s, Ant and Lauren, for handling more than you signed up for with grace, deftness, and

suavity; to Susan for her bountiful knowledge, calm and collected demeanor, and mothering

tendencies; to Bill, for without him none of this would have been possible: thank you.

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