Download MAPPING THE SPATIAL CONFIGURATION AND SEVERITY OF

MAPPING THE SPATIAL CONFIGURATION AND SEVERITY OF GIRAFFE SKIN
DISEASE IN RUAHA NATIONAL PARK, TANZANIA
By
Arthur Bienvenu Muneza
A THESIS
Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of
Fisheries and Wildlife – Master of Science
2016
ABSTRACT
MAPPING THE SPATIAL CONFIGURATION AND SEVERITY OF GIRAFFE SKIN
DISEASE IN RUAHA NATIONAL PARK, TANZANIA
By
Arthur Bienvenu Muneza
Giraffe numbers, have dropped by about 40% in the last 20 years, making giraffes a species of
conservation concern. In the same period of time, a skin disease has been observed in numerous
giraffe populations across Africa. The disease, commonly referred to as giraffe skin disease
(GSD), manifests as lesions, wrinkled skin, and encrustations that can affect the limbs, shoulder
or neck of giraffes. Giraffe skin disease may hinder movement causing increased susceptibility to
predation. In chapter 1, I reviewed GSD cases from literature reports and surveying efforts of
individuals working with giraffes in the wild and in captivity in order to compile a database of
known GSD cases. I detected variation in the manifestation, prevalence and severity of GSD in
sub-Saharan Africa and giraffe populations in captivity. In chapter 2, I used photographic
capture-recapture surveys via road-based transects in Tanzania’s Ruaha National Park to develop
a database of spatially-explicit giraffe images. I used WildID to process these photos for
individual identification and fitted spatial capture-recapture models to predict the spatial
configuration of giraffe abundance and GSD prevalence within the study area. My results
indicated that >86% of the giraffe population showed signs of GSD, which is the highest
prevalence of the disease in Africa. With vast areas of Sub-Saharan Africa still without
information on GSD, researching the prevalence and conservation impacts of this disease should
be a priority. I also discuss the implications of this research for conservation of threatened
species with an emphasis on disease ecology and vulnerability to predations, and more broadly,
for wildlife conservation.
ACKNOWLEDGEMENTS
I am very grateful to the people who contributed to this research, whose support and input
made this work possible and as unproblematic as possible. I would like to thank my academic
supervisor Robert Montgomery for his mentorship, patience, and guidance to achieve my
academic goals and embrace every challenge. I am very thankful to my graduate committee
members Gary Roloff and Jerry Urquhart for their valuable input and feedback. I am also
thankful to Amy Dickman, Julian Fennessy, Daniel Linden, and David Macdonald for lending
their expertise in this study. Many thanks my colleagues in the RECaP laboratory who provided
useful feedback to make this work easier and were a source of motivation.
Generous financial support for this research was provided by the MasterCard Foundation
Scholars Program at Michigan State University (MSU), RECaP Laboratory at MSU, the Giraffe
Conservation Foundation, the Leiden Conservation Foundation, the American Society of
Mammologists, and Roger Williams Zoo. I thank R. Glew, I. Kalumbu, and P. Croom among
others for administration of the MCF Graduate Scholars Fellowship.
I would like to thank S. Lipenga, M. Kimaro, N. Zuberi, A. Msago, J. Chambulila, U.
Mgogo, G. Kimathi, R. Lipenga, S. Enock, G. Sedoyeka, B. Lawa, D. Bora, P. Rogers, and all
the staff at Ruaha Carnivore Project and Ruaha Lion Guardians for their incredible support and
participation in data collection, and making my time in Ruaha extremely enjoyable. I extend my
gratitude to M. Brown, M. Castles, P. Clark, C. Pacho, P. Coppolillo, Chester Zoo, C. van
Wessem (Paignton Zoo), P. Seeber, A. Ganswindt, C. Riehm, R. Van Beek (Oregon Zoo), and
K. McQualter for contributing photos to this thesis. I also recognize the assistance provided by
COSTECH, TANAPA and TAWIRI officials in making this research possible.
iii
Thank you Georgina Montgomery and Olivia Montgomery for being a permanent source
of joy and encouragement during my time in East Lansing. I would like to thank my friends in
the MasterCard Foundation Scholars Programme, in particular J. Vareta, A. Kakpo, C. Latona, E.
Ansah, F. Uwimbabazi, J. Awadu, R. Kaihula, C. Gapare, among others, who offered different
perspectives and for their motivation. I am grateful to the Applied Forest and Wildlife Ecology
Lab at MSU for their company and advice. I would like thank Tom and Kathy Leiden, and the
Adams Family for their support and encouragement. Lastly, I would like to thank my father
Félicien Murego and two brothers, Felix Kwizera and Pierre Muhoza for bringing out the best in
me with their guidance and motivation.
iv
TABLE OF CONTENTS
LIST OF TABLES ......................................................................................................................... vi
LIST OF FIGURES ...................................................................................................................... vii
INTRODUCTION .......................................................................................................................... 1
REFERENCES ............................................................................................................................ 3
CHAPTER 1 ................................................................................................................................... 5
REGIONAL VARIATION OF THE MANIFESTATION, PREVALENCE, AND SEVERITY
OF GIRAFFE SKIN DISEASE: A REVIEW OF AN EMERGING DISEASE IN WILD AND
CAPTIVE GIRAFFE POPULATIONS .......................................................................................... 5
Abstract ....................................................................................................................................... 5
1.1. Introduction ...................................................................................................................... 6
1.2. Methods ............................................................................................................................ 9
1.3. Results ............................................................................................................................ 10
1.3.1. Review of skin diseases in giraffe populations ....................................................... 10
1.3.2. Variation in the anatomical location of GSD lesions.............................................. 11
1.3.3. Spatial variation in prevalence of GSD .................................................................. 12
1.3.4. Spatial variation in severity of GSD ....................................................................... 14
1.4. Discussion ...................................................................................................................... 15
Acknowledgements ................................................................................................................... 23
APPENDIX ............................................................................................................................... 24
REFERENCES .......................................................................................................................... 39
CHAPTER 2 ................................................................................................................................. 45
EXAMINING DISEASE PREVALENCE FOR SPECIES OF CONSERVATION CONCERN
USING NON-INVASIVE SPATIAL CAPTURE-RECAPTURE TECHNIQUES ..................... 45
Abstract ..................................................................................................................................... 45
2.1. Introduction .................................................................................................................... 46
2.2. Methods .......................................................................................................................... 49
2.2.1. Study area .................................................................................................................... 49
2.2.2. Vehicle-based photographic surveys ........................................................................... 50
2.2.3. Spatial Capture Recapture ........................................................................................... 51
2.3. Results ............................................................................................................................ 54
2.4. Discussion ...................................................................................................................... 56
Acknowledgements ................................................................................................................... 60
APPENDIX ............................................................................................................................... 61
REFERENCES .......................................................................................................................... 67
CONCLUSION ............................................................................................................................. 73
REFERENCES .......................................................................................................................... 75
v
LIST OF TABLES
Table 1.1. List of sources that reference descriptions of skin diseases in populations of wild
giraffe…………………………………………………………………………………25
Table 1.2. Areas where skin disorders have been observed in giraffe subspecies. The location of
GSD lesions on the body of affected individuals is indicated when applicable………27
Table 1.3. Fungal species identified by Epaphras et al. (2014) that are suspected to be involved in
the pathology of giraffe skin disease………………………………………………….28
Table 1.4. Areas where signs of GSD have been assessed but not been detected in the local
giraffe population……………………………………………………………………..29
Table 2.1. List and direction of 2015 survey routes in Ruaha National Park, Tanzania. The
direction was determined randomly from the start point on a given survey route and
the day of survey is counted from the first day a survey route was successfully
completed……………………………………………………………………………..62
Table 2.2. Parameter estimates (median and 95% credible interval) from the spatial capturerecapture model of adult and subadult giraffes in Ruaha National Park, Tanzania in
2015. Parameters include probabilities for individual attributes such as population
membership (ψ), sex (ψmale), age class (ψsubad), signs of GSD (ψGSD), and number of
legs with severe lesions (φk); log-linear regression coefficients for the encounter rate
(α) and the scale parameter of the half-normal detection function (δ); and derived
parameters of population size (N) and density (D) per km2…………………………..63
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LIST OF FIGURES
Figure 1.1. Distribution of giraffe (Giraffa camelopardalis) subspecies and giraffe skin disease in
Sub-Saharan Africa………………………………………………………………..30
Figure 1.2. Spatial variation in the manifestation of GSD in different giraffe populations. Panels
a, b, c: GSD in Murchison Falls National Park, Uganda; panels d, e, f: GSD in Ruaha
National Park, Tanzania; panel g: GSD in Hoarusib River, Kunene Region, Namibia;
panel h: GSD in Etosha National Park, Namibia; panel i: GSD in Kruger National
Park, South Africa; panels j, k, l: GSD in Chobe National Park, Botswana; panel m:
GSD in Hwange National Park, Zimbabwe; panel n: GSD in Oregon Zoo, Oregon,
USA; panel o: GSD in B. Bryan Preserve, California, USA……………………......31
Figure 1.3. Variation in the severity of GSD in two distinct giraffe populations. Panels a. b, c:
mild, moderate and severe GSD in Rothschild’s giraffes (G. c. rothschildi) in
Murchison Falls National Park, Uganda and panels d, e, f: mild, moderate and severe
GSD in Masai giraffe (G. c. tippelskirchi) in Ruaha National Park, Tanzania……....34
Figure 1.4. Variation in the anatomical location of GSD lesions. The x-axis represents the
number of times the GSD lesions were recorded in different study sites for a given
anatomical location…………………………………………………………………..35
Figure 1.5: Secondary infections, characterized by inflammations, in giraffe populations in
Ruaha National Park, Tanzania………………………………………………………36
Figure 1.6. Manifestation of giraffe skin disease in a female Rothschild’s giraffe (G. c.
rothschildi) before (a) and after (b) washings using 1:50 dilute chlorhexidine solution
in Paignton Zoo Environmental Park, England……………………………………...37
Figure 1.7. Unidentified skin lesions observed in wild and captive populations of giraffe. These
lesions are suspected to be related to GSD. Panel a: lesions on an Angolan giraffe (G.
c. angolensis) in Passage Valley, Central Kalahari Game Reserve in Botswana; panel
b: giraffe ear disease on a Masai giraffe (G. c. tippelskirchi) in Ruaha National Park,
Tanzania; panel c: otitis on a Masai giraffe (G. c. tippelskirchi) in Ruaha National
Park, Tanzania; panel d: lesions on an Angolan giraffe (G. c. angolensis) in the
central part of Etosha National Park, Namibia; panels e, f: blisters and lesions on the
lower leg and foot of a Rothschild’s giraffe (G. c. rothschildi) in Chester Zoo,
England………………………………………………………………………………38
Figure 2.1. Survey routes in the sampling area in Ruaha National Park, Tanzania. The map only
shows the road network that was used for the survey and each circuit is represented
by a different color…………………………………………………………………...64
Figure 2.2. User interface of Wild-ID software showing right-side image of interest (top left and
bottom left), active window (bottom right) and potential matches (top row and
arranged from right to left in a descending order of rank score)…………………….65
vii
Figure 2.3. Predictive map of realized giraffe density and GSD incidence in the survey area of
Ruaha National Park, Tanzania in 2015. Using SCR models, the plot shows potential
areas of GSD hotspot and higher centers of activity. Grid cell resolution was 2 km × 2
km……………………………………………………………………………………66
viii
INTRODUCTION
Giraffes (Giraffa carmelopardalis), the world’s tallest mammals and largest ruminants,
are widely appreciated for their striking appearance and beautiful coat patterns. For these
reasons, giraffes are commonly associated with zoos and yet, relatively little is known of their
natural ecology (Dagg, 2014; Bercovitch and Berry, 2012). With their elongated neck, long legs,
and a prehensile tongue, giraffes are specially adapted to capitalize on resources that are out of
reach for other large herbivores and therefore play an important role in the ecosystem as
megafauna (Dagg, 2014). They are major seed dispersers of Acacia nilotica, Acacia karroo, and
Acacia tortilis and they also make plant resources more accessible, via browsing pressure, which
can promote growth of new forage (Miller, 1996). For instance, moderate browsing by giraffes
has been shown to stimulate the production of shoots in certain acacia species (Du Toit et al.,
1990) and flower predation by giraffes encourages nectar production (Flemming et al., 2006),
which is an important food source for three species of ants that protect trees from pests like stemboring beetles (Palmer et al., 2008). Finally, giraffes, particularly immature animals, are prey for
several species of carnivore (Hayward, 2006; Hayward et al., 2006). Thus, giraffes play a critical
role in the regulation and balance of trophic interactions and ecosystem health (Giraffe
Conservation Foundation, 2013).
However, giraffe populations across sub-Saharan Africa are at risk mostly due to habitat
fragmentation, and poaching and snaring (Giraffe Conservation Foundation, 2013). In addition to
these anthropogenic threats, various skin diseases have recently begun to affect adult and
subadult giraffe throughout their range and pose an important risk to giraffe conservation.
Broadly, the skin diseases affecting several populations of giraffe have been collectively referred
to as Giraffe Skin Disease (GSD). Some have suggested that severe GSD can lead to lower leg
1
lameness making adult giraffes particularly vulnerable to lion predation (Anon, 2012; Epaphras
et al., 2012). However, detailed analyses of these processes have yet to occur. In the past 30
years, the number of giraffes has plummeted by ~40% to an estimated 90,000 free-ranging
giraffe and according to the International Union for the Conservation of Nature, the general trend
of giraffe populations across Africa is decreasing. Despite this documented decline in giraffe
abundance, little research has been conducted on giraffes, especially the role of disease in the
decrease of giraffe populations.
This thesis aims to provide much-needed baseline data of a skin disease that was first
observed in giraffe populations in Murchison Falls National Park, in north-western Uganda 20
years ago (Kalema, 1996) and yet very little is currently known of the disease or its effects on
giraffes. In chapter 1, I assessed peer-reviewed publications and unpublished reports, conducted
an online survey sent to researchers, veterinarians and managers working with giraffes in order
to produce a database of GSD incidences across Africa. Using these data, I report on the
variation in the manifestation of GSD, and assess the spatial variation of the prevalence and
severity of GSD across Sub-Saharan Africa. In chapter 2, I conducted non-invasive surveys to
identify individual giraffes, based on their unique coat patterns and fit spatial capture-recapture
models to estimate the prevalence of GSD in the giraffe population of Ruaha National Park and
predict the proportion of the giraffe population exhibiting GSD. This study provides data on the
spatial configuration of GSD in sub-Saharan Africa, the population size and distribution of
giraffe populations in Ruaha National Park and information for stakeholders on the use of noninvasive survey techniques to estimate the prevalence of a disease for wildlife conservation.
2
REFERENCES
3
REFERENCES
1) Anon. 2012. Research study needed for giraffe skin disease in Ruaha National Park,
Tanzania. Giraffa 6:24
2) Bercovitch, F. B. and P. S. M. Berry. 2012. Herd composition, kinship and fission–fusion
social dynamics among wild giraffe. African Journal of Ecology 51 (2):206 – 216
3) Dagg, A. I. 2014. Giraffe: Biology, Behaviour and Conservation. New York, Cambridge
University Press. ISBN 978-1-107-03486-0
4) Du Toit, J. T., J. P. Bryant, and K. Frisby 1990. Regrowth and Palatability of Acacia shoots
following pruning by African savanna browsers. Ecology 71(1):149 – 154
5) Epaphras, A. M., E. D. Karimuribo, G. D. Mpanduji and E. G. Meing’ataki. 2012.
Prevalence, disease description and epidemiological factors of a novel skin disease in
Giraffes (Giraffa Camelopardalis) in Ruaha National Park, Tanzania. Research Opinions in
Animal and Veterinary Sciences 2(1):60 – 65
6) Fleming, P.A., S.D. Hofmeyr, S.W. Nicolson and J.T. du Toit. 2006. Are giraffes pollinators
or flower predators of Acacia nigrescens in Kruger National Park, South Africa? Journal of
Tropical Ecology 22:247 – 253
7) Giraffe Conservation Foundation. 2013. Africa’s Giraffe (Giraffa camelopardalis): A
conservation guide. Black Eagle Media. Western Cape, South Africa
8) Hayward, M. W. 2006. Prey preferences of the spotted hyaena (Crocuta crocuta) and degree
of dietary overlap with the lion (Panthera leo). Journal of Zoology 270:606 – 614
9) Hayward, M. W., P. Henschel, J. O’Brien, M. Hofmeyr, G. Balme and G. I. H. Kerley. 2006.
Prey preference of the leopard (Panthera pardus). Journal of Zoology 270:298 – 313
10) Kalema, G. 1996. Investigation of a skin disease in giraffe in Murchison Falls National Park.
Uganda National Parks. Kampala, Uganda.
11) Miller, M.F. 1996. Dispersal of Acacia seeds by ungulates and ostriches in an African
Savanna. Journal of Tropical Ecology 12 (3):345 – 356
12) Palmer, T.M., M.L. Stanton, T.P. Young, J.R. Goheen, R.M. Pringle and R. Karban. 2008.
Breakdown of an Ant-Plant mutualism follows the loss of large herbivores from an African
Savanna. Science 319 (11):192 – 195
4
CHAPTER 1
REGIONAL VARIATION OF THE MANIFESTATION, PREVALENCE, AND
SEVERITY OF GIRAFFE SKIN DISEASE: A REVIEW OF AN EMERGING DISEASE
IN WILD AND CAPTIVE GIRAFFE POPULATIONS
Abstract
Large mammals have drastically declined in the past few decades yet we know little
about their ecology. Giraffe numbers for instance, have dropped by more than 40% in the last 15
years and recently, a skin disease, has been observed in numerous giraffe populations across
Africa. The disease(s), commonly referred to as giraffe skin disease (GSD), manifests as lesions,
wrinkled skin, and encrustations that can affect the limbs, shoulder or neck of giraffes. Here, I
review GSD cases from literature reports and surveying efforts of individuals working with
giraffes in the wild and in captivity. The aim of this review was to describe spatial variation in
the anatomical location of lesions, prevalence, and severity of GSD. In total, I retrieved 16
published sources that referenced GSD and I received 63 respondents to my survey. I found that
GSD has been observed in 13 protected areas across 7 countries in Africa and in 11 out of 48
zoos distributed across 6 countries. The prevalence of GSD in wild populations ranged from 2%
to 80% of observed giraffes. Although little research to date has focused on GSD, my review
reveals that the disease is more prevalent than initially thought and more severe in some areas
than previously assumed. With vast areas of Sub-Saharan Africa still without information on
GSD, researching the prevalence and conservation impacts of this disease should be a priority. I
propose broader and longer-term studies to further describe and comprehend the effects of GSD
on giraffe vital rates among populations in the wild and in captivity.
5
1.1.
Introduction
Large mammal populations have plummeted in recent times (Ceballos, 2005). Between
1970 and 2005, there was a 59% decrease in the population abundance of large African
mammals (Craigie et al., 2010). This decline in large mammal populations has been attributed to
both biotic and abiotic factors (Cardillo et al., 2005). For example, infectious diseases can pose a
substantial risk to populations of threatened species (Karimuribo et al., 2011): rinderpest has
caused massive mortality events for numerous species of African ungulates including Cape
buffalo (Syncerus caffer), eland (Taurotragus oryx), and kudu (Tragelaphus spp; Normile,
2008). Ethiopian wolves (Canis simensis) are threatened by rabies (Randall et al., 2006) and
canine distemper, which has a fatality rate that is second only to that of the aforementioned
disease, has been reported in all families of terrestrial carnivores (Deem et al., 2000; Mach et al.,
2008). Great apes such as the western lowland gorilla (Gorilla gorilla) and chimpanzee (Pan
troglodytes) have suffered drastic population declines associated with Ebola virus strains
(Huijbregts et al., 2003; Leroy et al., 2004). In the past 15 years, giraffe (Giraffa camelopardalis)
populations across Africa have declined by more than 40% (Giraffe Conservation Foundation
[GCF], 2013). The extent to which diseases have contributed to the decline of giraffe populations
is currently unknown.
Currently, there are 9 recognized subspecies of giraffe distributed across sub-Saharan
Africa (Fig. 1.1), though ongoing DNA analysis seeks to clarify the subspecies and species
divisions (Bock et al., 2014; GCF, 2013; Fennessy et al., 2013). The International Union for the
Conservation of Nature’s (IUCN) conservation statuses of these 9 giraffe subspecies vary,
though most are considered to be declining (Dagg, 2014; GCF, 2013). The West African giraffe
(G. c. peralta) and Rothschild’s giraffe (G. c. rothschildi), for instance, are both listed as
6
Endangered on the IUCN Red List (Fennessy and Brenneman, 2010; Fennessy and Brown, 2010,
GCF, 2010). The remaining subspecies, and consequently giraffe at the species-level, will be
recommended to be listed as Threatened on the IUCN Red List in 2016 (J. Fennessy pers. com.).
Although giraffe are a common captive animal in zoos across the world, there is very little
information describing the population dynamics, ecology, and behavior of wild-living giraffe
populations (Dagg, 2014). Despite this dearth of information, it is well understood that illegal
hunting, habitat fragmentation, and human encroachment are causally linked to the
fragmentation and decline of giraffe populations across Africa (Dagg, 2014; GCF, 2013).
However, the effect of disease on the population trajectories of these different giraffe subspecies
while potentially significant is poorly documented.
Giraffe experience a variety of skin disorders. For example, giraffe ear disease causes
wounds and lesions on the outer ear (Karimuribo et al., 2011). Yellow-billed (Buphagus
africanus) and red-billed (B. erythrorhynchus) oxpeckers are thought to be involved in the
pathology of giraffe ear disease (Karimuribo et al., 2011). Lumpy skin disease is a viral disorder
from the family Poxviridae which affects a variety of ungulates (Hunter and Wallace, 2001).
Much is known about lumpy skin disease because it is a common disease among livestock
(Davies, 1991; Woods, 1988; Young, 1970). Within the past 25 years however, another skin
disease has emerged in giraffe populations throughout Sub-Saharan Africa. This disease, which
has been generically referred to as giraffe skin disease (GSD) by researchers and veterinarians
who have studied the disease in East Africa (Epaphras et al., 2012; Karimuribo et al., 2011),
manifests as chronic and severe scabs, wrinkled skin, encrustations and dry or oozing blood on
the legs, shoulders, or necks of giraffes (Brown and Fennessy, 2014; Epaphras et al., 2012; Lee
and Bond, 2012). The wrinkled skin apparently becomes itchy, and affected animals have been
7
observed to regularly scratch affected regions against branches and trees (Epaphras et al., 2012;
Lee and Bond, 2012). Giraffe skin disease is an emergent disease, has only recently been
described in the literature, and is readily distinguishable from giraffe ear disease or lumpy skin
disease (Brown and Fennessy, 2014; see Dagg, 2014: pp 88; Epaphras et al., 2012; Kalema,
1996; Karimuribo et al., 2011; Lee and Bond, 2012). Across the geographic range of giraffes,
GSD appears to exhibit variation in its manifestation. In Tanzania, the disease afflicts the legs of
giraffe (Epaphras et al., 2012; Karimuribo et al., 2011; Lee and Bond, 2012) whereas in other
areas, such as northern Uganda, GSD can appear on the neck and upper torso (Brown and
Fennessy, 2014). The etiological agent of the disease(s) has not yet identified and thus whether
the spatial variation in GSD is due to different infectious agents or not remains unknown.
Preliminary investigations on giraffe populations in Ruaha National Park, Tanzania suggest
involvement of ticks (Anon., 2012) or nematodes (Karimuribo et al., 2011), although these
reports are unconfirmed. Some affected giraffe in Tanzania have been reported to be lame,
potentially increasing their vulnerability to poaching or predation (Epaphras et al., 2012; Lee and
Bond, 2012). To date, there is no information on the effect of GSD on the survival and
reproduction of giraffe.
Given the lack of information on GSD, a comprehensive literature review was warranted.
Here I report on the variation in the manifestation of GSD, and assess the spatial variation of the
prevalence and severity of GSD across Sub-Saharan Africa. Through an assessment of peerreviewed publications, unpublished reports, personal communication and surveys, I produced a
current database of GSD incidences across Africa, mapped its prevalence and impacts, and
provided recommendations for the management of this disease for giraffe conservation.
8
1.2.
Methods
To obtain data on GSD and its variations across Africa, I conducted an extensive
literature review of published information via five major online literature databases. These
included: JSTOR, PubMed, SAGE, Web of Science and Google Scholar. The key words for
searches included combinations of: Giraffe Skin Disease; Giraffa camelopardalis; lesions on
giraffe; subspecies names; and the country and study site names for the different giraffe
populations across Africa. I filtered database hits by title, then by abstract, and finally by
reviewing the full paper placing no limitations on year of publication. I rejected hits that did not
describe any form of skin disease in giraffe and hits that described skin diseases that were well
documented over a large variety of mammalian taxa such as mange.
I also communicated directly with individuals studying or working with giraffe both in
the wild and in captivity. I published a call in the IUCN Giraffe and Okapi Specialist Group and
Giraffe Conservation Foundation’s (GCF) Giraffid bi-annual journal in May 2015 detailing my
intent to better understand the prevalence of GSD (Montgomery and Muneza, 2015). I contacted
researchers, ecologists, veterinarians, conservation officials, and managers within the network of
GCF contacts and those that are part of IUCN’s Giraffe and Okapi Specialist Group. The Giraffe
and Okapi Specialist Group kindly forwarded my request to other professionals known to be
studying giraffe within their networks. I asked respondents to fill in a short survey. This survey
was developed to understand better the variation in the spatial configuration of GSD and was
approved by Michigan State University’s Institutional Review Board (IRB) under IRB
application number: x15-w435e, and i048681. I requested that the respondents provide as much
information as possible describing any incidences where they observed affected giraffe.
Specifically, I asked respondents to provide photographs, reports or published papers that
9
described mild, moderate and severe GSD in their study area, described the distribution and color
of lesions on affected giraffe, and provided an estimation of the prevalence of GSD in their study
area. Information garnered from this survey included location, prevalence, and severity.
1.3.
Results
1.3.1. Review of skin diseases in giraffe populations
From my literature review, I found 16 written sources directly relating to skin diseases in
giraffe populations (Table 1.1). Lumpy skin disease was described in 5 papers, while 2 papers
described papillomavirus lesions in giraffe. These 5 papers were not considered further in this
GSD review because lumpy skin disease is a known disease that is readily distinguishable from
GSD. In total, I found 8 sources that provided descriptions of GSD in wild-living giraffe
populations. These 8 sources included 2 published papers, 5 unpublished reports, and 1 paper
calling for research proposals. I received 63 responses to my questionnaire survey from which I
retrieved one source, an unpublished report, referencing GSD. Here, I review the information
garnered from a total of 9 sources and 63 respondents on GSD.
The majority of respondents (76%, n = 48) to the survey were from zoos. Over 30% (n =
20) of the respondents observed evidence of skin disorders in giraffe. Among these reported
cases of skin disorders, 70% (n = 14) were GSD cases and 30% (n = 6) were cases of lumpy skin
disease. Data derived from the literature review and questionnaire survey, identified that GSD is
present both in wild and captive giraffe populations (Table 1.2). I found GSD cases in 13
national parks and game reserves across 7 countries in sub-Saharan Africa (Fig. 1.1), and in 11
zoos distributed across 6 countries. In total, GSD was observed in 6 of the 9 (67%) giraffe
subspecies, and in 4 giraffe subspecies in wild populations: Masai giraffe (G. c. tippelskirchi),
10
Rothschild’s giraffe (G. c. rothschildi), Cape giraffe (G. c. giraffa), and Angolan giraffe (G. c.
angolensis). Giraffe skin disease was also observed in 4 subspecies (Table 1.2) of captive
populations of giraffe: Kordofan giraffe (G. c. antiquorum), Masai giraffe (G. c. tippelskirchi),
Reticulated giraffe (G. c. reticulata), and Rothschild’s giraffe (G. c. rothschildi).
1.3.2. Variation in the anatomical location of GSD lesions
The 7 Sub-Saharan African countries where GSD has been detected are Uganda, Kenya,
Tanzania, Zimbabwe, Botswana, Namibia and South Africa (Fig. 1.1). Giraffe skin disease was
first reported in Chobe and Pakuba regions, western Murchison Falls National Park, Uganda in
the early 1990s (Kalema, 1996). In Uganda, GSD in Rothschild’s giraffe is characterized by
crusty, greyish-brown lesions that are irregular in shape and size, ranging from 10-15cm in
diameter (Brown and Fennessy, 2014; Kalema, 1996). The lesions initially start as one patch and
can spread to as many as 4 patches (Fig. 1.2), which occur either at the base of the neck, along
the neck, or on the sides next to the shoulder (Fig. 1.3; Brown and Fennessy, 2014; Kalema,
1996). However, lesions on the back hip and hip joint can also form more than 4 patches of
GSD. The first observations of GSD in Tanzania occurred in 2000 from Ruaha National Park in
the southern part of the country (Epaphras et al., 2012; Mpanduji et al., 2011). The disease has
since been documented in northern Tanzania, from the Serengeti National Park, Tarangire
National Park, and Manyara Ranch Conservancy (Lee and Bond, 2012). Unconfirmed reports
suggest that GSD has also afflicted the giraffe populations in Mikumi National Park and Selous
Game Reserve (Brown and Fennessy, 2014). As was the case in Uganda, GSD lesions examined
in Tanzania were crusty and proliferative. They tended to start as small skin nodules of about 23cm in diameter with raised hair, that later become larger round or oval alopecic patches of 1016cm in diameter (Fig. 1.3; Epaphras et al., 2012; Mpanduji et al., 2011). In severely affected
11
giraffe, the skin develops wrinkles, scabs, scales and cracks with raw fissures (Fig. 1.2; Epaphras
et al., 2012; Epaphras et al., 2014). The lesions were observed on the forelimbs, hind limbs, hind
quarters, base of the neck, brisket area and on the sides next to the shoulder of examined Masai
giraffe in Tanzania (Fig. 1.2; Epaphras et al., 2012; Mpanduji et al., 2011).
In Lake Nakuru National Park and Soysambu Conservancy in Kenya, lesions were
observed on the legs of afflicted Rothschild’s giraffe. In Hwange National Park, Zimbabwe,
Chobe National Park, Botswana, and Kruger National Park, South Africa, the upper body of
affected Cape giraffe was covered with GSD lesions (Fig. 1.2). Lesions were also observed on
the pastern joints of the hind limbs of Angolan giraffe in the Hoarusib River in Namibia, while in
Etosha National Park, GSD lesions were seen on the carpal joints of the forelimbs of afflicted
individuals (Fig. 1.2). My results indicate that GSD was more commonly observed on the limbs
of giraffe populations that have been assessed thus far (Fig. 1.4).
In my survey, 22% (n = 11) observed GSD lesions in their respective captive giraffe
populations. Small lesions on the limbs, inner thigh, groin area or scrotum (Fig. 1.2) were
recorded in 63.6% (n = 7) of the zoos reporting GSD. Lesions on the upper body of giraffe were
found in 18.2% (n = 2) of GSD cases observed in zoos whereas lesions were observed on the
entire body and the head of afflicted individuals in 18.2% of the reported cases.
1.3.3. Spatial variation in prevalence of GSD
I detected considerable variation in the prevalence of GSD across regions in sub-Saharan
Africa. A preliminary study in Murchison Falls National Park, Uganda identified that 19% (n =
71) of all observed giraffe (n = 371) were afflicted by GSD (Brown and Fennessy, 2014). Giraffe
skin disease cases were more common in adult giraffe (91% of the observed cases of GSD).
12
From these cases of GSD, 24% of the affected individuals were male and 23% were female. My
questionnaire survey suggests a slightly higher prevalence of GSD in Murchison Falls National
Park (M. Brown, pers. com.), with 23% of all observed giraffe reportedly affected (Fig. 1.1). The
reported prevalence of GSD in adult giraffe was markedly higher than stated in Brown and
Fennessy (2014), with 53% of adult male giraffe and 47% of adult females reportedly affected.
Further, affected adult giraffe accounted for 97% of the observed GSD cases. Giraffe skin
disease was reported to be most prevalent in the west side of Murchison Falls National Park with
giraffe subpopulations in the central and eastern part of the Park showing fewer visible signs of
GSD (Kalema, 1996; Brown and Fennessy, 2014).
In Tanzania, 79.8% (n = 109) of all Masai giraffe in Ruaha National Park had GSD, with
rates >90% reported for adult males and females (Epaphras et al., 2012; Mpanduji et al., 2011).
These are the highest rates of GSD detected in this review. The prevalence of the disease in
Ruaha National Park was >80% in all sections of the Park, except for the eastern portion where
only 37.5% of observed animals were affected by GSD (Epaphras et al., 2012). With 61% (n =
159) of all observed animals affected by GSD, Tarangire National Park had the second-highest
rate of GSD cases in Tanzania detected in this review (Lee and Bond, 2012). In contrast,
Serengeti National Park and Manyara Ranch Conservancy had a prevalence rate 23% (n = 53)
and 10% (n = 145), respectively of all observed animals (Fig. 1), and no cases of GSD were
observed in Arusha National Park, Lake Manyara National Park or Ngorongoro Conservancy
Area (Lee and Bond, 2012).
In Namibia, GSD was detected in the eastern portion of Etosha National Park, and in
Hoarusib River, northwestern Kunene Region. Only 2% of the examined giraffe in far
northwestern Namibia were affected by GSD while no studies have been conducted to estimate
13
the prevalence of GSD in Etosha National Park. Similarly, GSD was detected in numerous other
populations and countries but there is no research to quantify the prevalence rate of the disease:
Lake Nakuru National Park and Soysambu Conservancy in Kenya, Selous Game Reserve and
Mikumi National Park in Tanzania, Hwange National Park in Zimbabwe, Chobe National Park
in Botswana, and Kruger National Park in South Africa (Fig. 1.1). Giraffe skin disease was
detected in captive populations of giraffe but only observed in one or two animals in each (Table
1.2). However, the entire giraffe population in Safaripark Beekse Bergen Zoo in the Netherlands
was affected. Similar to GSD cases in wild giraffe populations, the GSD cases in zoos
predominantly affected adult giraffe and no cases were detected in juveniles. There are areas
where the no signs of GSD have been observed in the giraffe population (Table 1.4)
1.3.4. Spatial variation in severity of GSD
The severity of GSD was variable between sites. In Ruaha National Park, 99% (n=91) of
all examined GSD cases were chronic lesions among which 51.7% of the affected individuals
had severe (skin wrinkles, scabs, scales cracks with raw fissures - not quantitatively defined)
lesions of GSD (Epaphras et al., 2012). Even though the majority of GSD lesions in Ruaha
National Park were chronic, most of the affected individuals (87.1%) had a normal gait
(Epaphras et al., 2012). The rest were either walking ‘very carefully’ (2.9%) or had a ‘stiff gait’
(4.4%), and 2.9% of the affected had a form of lameness (Epaphras et al., 2012). Severely
affected animals were reluctant to use their legs, standing at one place for long periods, and when
disturbed, showed signs of lameness (Epaphras et al., 2012; Lee and Bond, 2012). In Namibia’s
Hoarusib River, a male giraffe with GSD was seen limping, and did not move far during a few
days of observations. However, a female with GSD in the same park did not seem to be affected.
14
Giraffe with severe GSD have shown signs of pruritus and frequently rubbed against
branches of smaller bushes and trees in several study areas in Tanzania (Epaphras et al., 2012;
Lee and Bond, 2012). Giraffe with poor or fair body condition due to GSD lesions were observed
in 11% of affected giraffe in Ruaha National Park (Epaphras et al., 2012). Giraffe skin disease
may increase vulnerability to secondary infections (Epaphras et al., 2012; Lee and Bond, 2012;
Mpanduji et al., 2011), which have been observed manifesting as inflammations and abscesses
on the limbs of affected individuals (Fig. 1.5). No studies have been conducted to determine the
extent to which these infections affect giraffe fitness and condition.
It has been suggested that up to 17 different fungal species (Table 1.3) could be involved
in the pathology of GSD but the specific causative fungus has not been identified (Epaphras et
al., 2014). Nematodes are also suspected to be involved in the pathology of GSD (Karimuribo et
al., 2011) but laboratory tests could not identify the specific nematode (Epaphras et al., 2014).
Thus, GSD may be caused by a nematode then complicated by secondary fungal infection
(Epaphras et al., 2014).
1.4.
Discussion
This review revealed that GSD is an understudied and little known disease. I retrieved
just 9 sources referencing GSD and only two of these were published in peer-reviewed journals.
Though GSD was first described in the mid 1990s in Uganda (Kalema, 1996) where it affected
one of the five remaining viable populations of Endangered Rothschild’s giraffe (Brenneman et
al., 2009), the disease has not yet received international scientific attention. A large portion of
the available information that describes GSD is scattered in reports developed by various
management entities and stakeholders. However, accessing these data can be difficult due to
15
various factors, especially in the case of wild populations of giraffe. This is evident from the fact
that there is a large area within the range of giraffe subspecies in Sub-Saharan Africa where the
status of GSD and other skin diseases is currently undetermined. The descriptions of GSD in this
review are derived primarily from preliminary studies (see Epaphras et al., 2012; Kalema, 1996;
Karimuribo et al., 2011; Mpanduji, 2011). My study identified that GSD occurs in areas
previously not described in the literature including Etosha National Park and northwestern
Namibia, Hwange National Park in Zimbabwe and Chobe National Park, Botswana. I anticipate
that the reported cases of GSD will likely increase as conservation attention for giraffe increases
and scientists gather more data on the ecology of this iconic species (Bock, et al., 2014; Dodson,
2015; Seeber et al., 2012).
I found that GSD lesions were located on different anatomical locations of affected
individuals in numerous sub-populations across sub-Saharan Africa (Fig. 1.4). However, across
sites there were similarities in size and appearance of the lesions suggesting that it could be the
same infection in some instances (Fig. 1.2). As an example, Kalema (1996) noted that the lesions
observed on the necks of Rothschild’s giraffe in Murchison Falls National Park, Uganda
measured 10-15cm in diameter and Epaphras et al. (2012) estimated that the diameter of the
lesions on the forelimbs of Masai giraffe in Ruaha National Park, Tanzania were 10-16cm.
Moreover, photos and descriptions from the northern parks in Tanzania (Tarangire, Serengeti and
Manyara Conservancy Ranch) matched the descriptions recorded in Ruaha National Park. This is
interesting given that the vegetation composition and landscape structure between northern and
southern Tanzania varies dramatically. The northern areas tend to be dominated by grasslands
while the southern areas consist of highlands, woodland grasslands and open woodlands (Pelkey
et al., 2000). Similar to the wild, manifestation of GSD in captivity also varied. Lesions were
16
observed on the limbs, testicles, upper body, head, and in one case, on the entire body of the
affected giraffe (Table 1.2). Also similar to wild populations, the lesions observed in captivity
tended to be relatively consistent in appearance, primarily differing in the number of patches.
Again, the etiology of GSD is yet to be determined, but these examples of GSD characterized by
crusty and proliferative lesions and wrinkled skin signify the occurrence of several forms of the
same disease (GSD).
Despite the fact that GSD can be common and is often severe in areas where it occurs,
this review demonstrates that there is high variation in the prevalence of the disease. In her
preliminary study, Kalema (1996) observed GSD in just a few giraffe in Murchison Falls
National Park, but by 2014 the disease was detected in 19% of the population (Brown and
Fennessy, 2014). Updated information reported in the structured surveys identified that GSD is
prevalent in as much as 23% of the giraffe population (M. Brown pers. comm.). What remains
unclear is whether this increase is attributable to the actual prevalence of the disease over time or
better and long-term surveying. Documenting the factors associated with the spread of the
disease is crucial to determining the extent to which it is communicable and to identify pathways
for potential treatments. For instance, some herbivores migrate between Kenya’s Masai Mara
Game Reserve and Serengeti National Park and Ngorongoro Conservation Area in Tanzania
(Boone, et al., 2006; Estes et al., 2006). I do not know whether these migrating species are
involved in the pathology of GSD. This is particularly important for mitigating the spread of the
disease given that 23% of the observed giraffe in Serengeti National Park are affected by GSD
while there are no reported cases of GSD reported in Ngorongoro (Lee and Bond, 2012), and the
status of GSD in the Masai Mara is unknown. Nonetheless, I am unaware of any reports of other
animals living in close proximity with giraffe that are affected by a disease like GSD (Kalema,
17
1996; Mpanduji, 2011; Epaphras et al., 2012). However, there is a filarial disease, which is
similar in appearance to GSD in white (Ceratotherium simum) and black (Diceros bicornis)
rhinos occurring in Meru National Park in Kenya, but affected rhinos recovered fully once
treated after 3 months (Mutinda et al., 2012).
Studying the pathology and epidemiology of GSD in the wild can be challenging since
giraffe maintain a fission-fusion social system (Bercovitch and Berry, 2012; Carter et al., 2013;
Leuthold, 1979). Such complex dynamics in group size and structure, and range of giraffe,
coupled with the fact that giraffe home ranges can vary from 5 km 2 in Lake Manyara National
Park, Tanzania (van der Jeugd & Prins 2000) to 1,950 km2 in northwestern Namibia (Fennessy,
2004) pose challenges in identifying and assessing both biotic and abiotic factors linked to the
infection. Nonetheless, the development of new technologies allows integration of geospatial
data, spatial statistics, and disease ecology to better study emerging diseases (Kitron, 1998,
Kistemann et al., 2002). I found that tissue samples, intending to examine the pathology of GSD,
have been collected three times. These efforts occurred in Ruaha National Park (Epaphras 2014)
and in two zoos (Paignton Zoo in England and B. Bryan Preserve in USA). In all cases tissue
cultures were collected in an effort to isolate the etiological agent of GSD but the tests were not
conclusive. In Ruaha National Park, 14 affected and 2 unaffected samples were collected and
skin biopsies and DNA sequencing tests were performed to identify the etiological agent linked
to GSD (Epaphras et al., 2014). The sequencing results of the samples indicated the presence of
more than one type of nematode but could not identify the specific species linked to GSD.
Similar tests on fungal isolates revealed the presence of a number of fungal spores (Table 1.3).
Among the fungal species identified, two were found in healthy giraffe (Epaphras et al., 2014).
The report concluded that GSD is caused by a nematode infection, then complicated further by
18
secondary fungal infections. In Paignton Zoo, samples were collected to check for fungal spores
and mites in both the affected female and male Rothschild’s giraffe. There were no pathogens
isolated in the male giraffe but there was pure growth of Aggregatibacter aphrophilus in the
female giraffe. The lesions were managed by using 6 washings of 1:50 dilute chlorhexidine
every 2-3 days and most scabs cleared in the male and initially the female looked better, but the
skin around the lesions appeared sweaty. A further 6 washings were performed and hair slowly
grew back over the lesions. After this treatment, there was no oozing and there was less visible
sweatiness of skin (Fig. 1.6). In B. Bryan Preserve, skin scrapes were analyzed but there were no
conclusive findings. The results did not show the presence of any infectious microbe but there
were high levels of a lanolin-based substance in the samples. In Safaripark Beekse Bergen Zoo
(Netherlands), GSD disappeared as soon as BoskosTM (WES Enterprises (Pty) Ltd, South
Africa) was introduced into the diet. BoskosTM is made from Acacia, Dichrostachus,
Combretum and Grewia spp., and contains 10% crude protein, maximum 35% fiber, minimum
2.5% fat and total digestible nutrients amounting to 60%. When BoskosTM was not in the diet
for 1-1.5years, the lesions would reappear again.
There is no information available describing the spread and effects of GSD on giraffe
sub-populations, which is crucial to the strategic management and conservation of giraffe. In the
first study of GSD, Kalema (1996) concluded that GSD was not an emergency at that time
because it was an isolated disease occurring in only a portion of the giraffe population in
Uganda. Since 1990, the disease has become more common throughout the range of giraffe.
Within the last few years, there have been several calls for additional long-term research to
further describe and understand the effects of GSD on the vital rates of giraffe populations
(Epaphras et al., 2012; Brown and Fennessy, 2014, Epaphras et al., 2014). There is reason to
19
believe that giraffe could be negatively affected by GSD. For instance, giraffe that are weakened
by starvation, harsh climatic conditions or compromised health (Hirst, 1969) are easier prey for
lion, especially given that giraffe are part of the preferred prey of lion (Hayward and Kerley,
2005). Therefore, it is crucial to understand the extent to which GSD affects giraffe-lion
interactions in areas where both species occur concurrently. While preliminary studies in Ruaha
(Epaphras et al., 2012) showed that the gait of affected individuals was not severely affected,
research should be dedicated to understanding the extent to which GSD affects the vital rates and
overall fitness of individuals afflicted by the disease to better assess their likelihood of survival.
As well as GSD, there are other emerging infections whose effects on the survival and vital
rates of giraffe are unknown. One of these infections, giraffe ear disease, which manifests as
lesions on the ear of affected giraffe (Fig. 1.7), is known to be complicated by oxpeckers (as may
GSD) but the etiological agent has not yet been identified (Karimuribo et al., 2011; Mpanduji et
al., 2011). Other skin disorders have been observed in Etosha National Park (M. Castles, pers.
comm) and the Passage Valley in Central Kalahari, Botswana (C. Pacho and S. Fennessy, pers.
comm). In Chester Zoo, UK, lesions appeared on the lower parts of the feet of one male giraffe.
The diagnosis at the time was pemphigus, a skin disorder characterized by watery blisters on the
skin. Corticosteroids were administered to counteract the effect of the lesions since the affected
giraffe had difficulty standing and moving but the treatment was unsuccessful. The lameness was
worse in the hind legs, and the giraffe exhibited trembling flanks. The giraffe was later
euthanized on the grounds of welfare due to uncontrollable pain. This underscores the need to
study the effects that diseases such as GSD have on both wild and captive populations of giraffe.
Emerging diseases, especially terminal illnesses, can lead to significant declines of freeranging wildlife populations. For instance, the Tasmanian devil facial tumor disease (FTD),
20
which first recorded in 1996, has led to a density decrease of up to 90% in some Tasmanian devil
(Sarcophilus harrisii) populations (McCallum et al., 2007, 2009). The lethal infectious cancer is
projected to occur across the entire range of Tasmanian devils in 5 to 10 years (McCallum et al.,
2007) and could likely lead to a disease-induced extinction of the world’s largest carnivorous
marsupial (Jones et al., 2007; McCallum et al., 2009). Other skin diseases have also decimated
wildlife populations; white nose syndrome (WNS) has led to a collapse of North American bat
species since its first observation in 2006 (Blehert et al, 2008; Frick et al., 2010), while
chytridiomycosis is associated with catastrophic declines of amphibians on a global scale
(Voyles et al., 2009). Research effort are ongoing to better understand the epidemiology of these
diseases (FTD, WNS, and chytridiomycosis) and their etiological agents, which have been
known to have 100% mortality rates in some cases (McCallum et al., 2009; Voyles, et al., 2009;
Frick et al., 2010). From the available literature so far, it is unknown whether GSD causes any
physiological changes in affected giraffe or is the cause of or leads to mortality.
This review demonstrates that there is a need for additional research on GSD including
the collection and appropriate analysis of samples from affected individuals. I recommend that
collaborative research to compare samples within and across giraffe populations to determine
whether the different manifestations of GSD are attributable to the same pathogen(s) and to
identify the pathways of infection. A combination of different molecular techniques producing
more specific results may show promise for GSD (Kuiken et al., 1999). Additional research on
GSD could potentially generate cures for the disease(s), as has occurred for other skin diseases.
Lumpy skin disease, for instance, has been extensively studied in livestock, which led to the
development of vaccines that have been successful in controlling the disease (Woods, 1988;
Davies, 1991; Coetzer and Tustin, 2004). Lumpy skin disease has been detected in both wild
21
and captive populations of giraffe (Table 1.2), but as far as I know, there is no study of the
disease in wild populations (Coetzer and Tustin, 2004; Fennessy 2004; Woods, 1988; Young,
1970). There are many questions that are still unanswered pertaining to the pathology,
epidemiology, and consequences of GSD. I do not know whether GSD is fatal to giraffes as this
has not been monitored in any setting. As shown through this study, there are still areas where
the status, severity or prevalence of GSD has not been determined (Fig. 1.1). I recommend that
studies should better understand the causative agent of GSD and the risk factors associated to the
disease. This will allow stakeholders in giraffe conservation to make effective management
decisions.
22
Acknowledgements
I thank IUCN SSC GOSG, WildCRU at the University of Oxford and the RECaP Laboratory at
Michigan State University (MSU) for guidance in preparation of this manuscript. Generous
support for this research was provided by the MasterCard Foundation Scholars Program at MSU,
the Giraffe Conservation Foundation, the Leiden Conservation Foundation and the American
Society of Mammologists. I thank R. Glew, I. Kalumbu, and P. Croom among others for
administration of the MCF Graduate Scholars Fellowship. I extend my gratitude to M. Brown,
M. Castles, P. Clark, C. Pacho, P. Coppolillo, Chester Zoo, C. van Wessem (Paignton Zoo), P.
Seeber, A. Ganswindt, C. Riehm, R. Van Beek (Oregon Zoo), and K. McQualter for
contributing photos to this manuscript.
23
APPENDIX
24
APPENDIX
Table 1.1. List of sources that reference descriptions of skin diseases in populations of wild
giraffe.
Study
period
1970
1976
Study area
Kruger National
Park (lab
experiment)
Kiboko
Country
South
Africa
Kenya
1988
1991
NAa
NAa
1996
2001
Murchison Falls
National Park
NAa
2004
NAa
20072008
2011
Kruger National
Park
NA
2011
Ruaha National
Park
2012
Ruaha National
Park
2012
Ruaha National
Park
2012 – Tarangire
Present National Park,
Manyara
National Park,
Manyara Ranch
Conservancy,
Ngorongoro
Conservation
Area, Serengeti
National Park,
Arusha National
Park
Regional
Regional
Uganda
Regional
Regional
South
Africa
Tanzania
Tanzania
Tanzania
Tanzania
Tanzania
Disease
Reference
LSD
Young, 1970
Papillomavirus
infection
Karstad and
Kaminjolo,
1978
Woods, 1988
Davies, 1991
Peer-reviewed
research paper
Kalema, 1996
Unpublished
report
Review paper
LSD
Lumpy Skin
Disease
Giraffe Skin
Disease
Lumpy Skin
Disease
Lumpy Skin
Disease
Papillomavirus
infection
Giraffe Skin
Disease
Giraffe Skin
Disease
Giraffe Skin
Disease
Giraffe Skin
Disease
Giraffe Skin
Disease
25
Hunter and
Wallace, 2001
Coetzer and
Tustin, 2004
van Dyk et al.,
2011
Karimuribo et
al., 2011
Mpanduji et al.
2011
Anon, 2012
Epaphras et
al., 2012
Lee and Bond,
2012
Type of
literature
Peer-reviewed
research paper
Review paper
Review paper
Book chapter
extract
Peer-reviewed
research paper
Review paper
Unpublished
report
Call for
proposals
Peer-reviewed
research paper
Unpublished
report
Table 1.1. (cont’d)
Study
period
2013
2014
2014
Study area
Ruaha National
Park
Murchison Falls
National Park
Ruaha National
Park
Country
Tanzania
Uganda
Tanzania
Disease
Reference
Giraffe Skin
Disease
Giraffe Skin
Disease
WCS, 2013
Giraffe Skin
Disease
*
Brown and
Fennessy,
2014
Epaphras et
al., 2014
Type of
literature
Unpublished
report
Unpublished
report
Unpublished
report
Paper analyzes studies conducted in multiple areas and aggregates findings in a systematic
review paper.
26
Table 1.2. Areas where skin disorders have been observed in giraffe subspecies. The location of
GSD lesions on the body of affected individuals is indicated when applicable.
Location
Country
Atherstone Nature Reservea
Chobe National Parkb
Entabeni Game Reservea
Etosha National Parka
Hoarusib River, Kunene Regiona
Hwange National Parkb
South Africa
Botswana
South Africa
Namibia
Namibia
Zimbabwe
Ithala National Parkb
Kruger National Parkb
Lake Nakuru National Parkc
Manyara Ranch Conservancyd
Murchison Falls National Parkc
Ruaha National Parkd
Selous Game Reserved
Serengeti National Parkd
Soysambu Conservancyc
Tarangire National Parkd
Banham Zood
Bronx Zooc
Columbus Zoo and Aquariumd
Flamingo Landc
Great Plains Zooe
Jacksonville Zoo and Gardense
South Africa
South Africa
Kenya
Tanzania
Uganda
Tanzania
Tanzania
Tanzania
Kenya
Tanzania
England
USA
USA
England
USA
USA
Type of
skin
disorder
LSD
GSD
LSD
GSD
GSD
LSD and
GSD
LSD
GSD
GSD
GSD
GSD
GSD
GSD
GSD
GSD
GSD
GSD
LSD
GSD
LSD
GSD
GSD
La Reserva del Castillo de las Guardase
Oregon Zooe
Paignton Zoo Environmental Parkc
Parc de Beauvale
Parco Natura Viva Garda Zoological Parkc
Royal Zoological Society of Antwerpf
Safaripark Beekse Bergenc
Spain
USA
England
France
Italy
Belgium
Netherlands
LSD
GSD
GSD
GSD
GSD
GSD
GSD
Location of lesions
NA
Upper body
NA
Limbs
Limbs
Upper body*
NA
Upper body
Limbs
Limbs
Neck
Limbs, neck
Limbs
Limbs
Limbs
Limbs
Limbs
NA
Limbs
NA
Limbs
Limbs, testicles, inner
thigh, upper body
NA
Limbs
Limbs
Head
Upper body
Upper body
Entire body
*Refers to location of GSD lesions. For this study, I did not include the location of lumpy skin
disease (LSD) lesions.
a
Cape giraffe (G. c. giraffa)
Angolan giraffe (G. c. angolensis)
c
Rothschild’s giraffe (G. c. rothschildi)
d
Masai giraffe (G. c. tippelskirchi)
e
Reticulated giraffe (G. c. reticulata)
f
Kordofan giraffe (G. C. antiquorum)
b
27
Table 1.3. Fungal species identified by Epaphras et al. (2014) that are suspected to be involved in
the pathology of giraffe skin disease.
Auerobasidium pullulons
Auerobasidium spp.
Aspergillus niger
Aspergillus fruticulosus
Aspergillus multicolor
Aspergillus sydrowii
Aspergillus versilor
Cochliobolus lunatus*
Emericella omanensis
Fungal species name
Epicoccum sorghum
Exsorohilum rostratum
Fennellia nivea
Fusarium equiseta
Penicillium citrinum
Penicillium commune*
Penicillium griseofulvum†
Phoma spp.
* Indicates fungal species that are also found in healthy giraffe.
†
Indicates fungal species with anti-inflammation properties.
28
Table 1.4. Areas where signs of GSD have been assessed but not been detected in the local
giraffe population.
Location
Amboseli National Park
Arusha National Park
Gambella National Park
Country
Kenya
Tanzania
Ethiopia
Garamba National Park
Democratic
Republic of Congo
Garden Route (Western Cape) South Africa
Laikipia and Samburu
Kenya
landscape
Lake Manyara National Park
Tanzania
Nairobi National Park
Kenya
Ngorongoro Conservation
Tanzania
Area
Sioma Ngwezi National Park Zambia
Tama Wildlife Reserve
Ethiopia
Tsavo West National Park
Kenya
29
Giraffe subspecies
Masai giraffe (G. c. tippelskirchi)
Masai giraffe (G. c. tippelskirchi)
Nubian giraffe (G. c.
Camelopardalis)
Kordofan giraffe (G. C.
antiquorum)
Cape giraffe (G. c. giraffa)
Reticulated giraffe (G. c.
reticulata)
Masai giraffe (G. c. tippelskirchi)
Masai giraffe (G. c. tippelskirchi)
Masai giraffe (G. c. tippelskirchi)
Thornicroft’s giraffe (G. c.
antiquorum)
Reticulated giraffe (G. c.
reticulata)
Masai giraffe (G. c. tippelskirchi)
Figure 1.1.
Distribution of giraffe (Giraffa camelopardalis) subspecies and giraffe skin disease in SubSaharan Africa.
30
Figure 1.2.
Spatial variation in the manifestation of GSD in different giraffe populations. Panels a, b, c: GSD
in Murchison Falls National Park, Uganda; panels d, e, f: GSD in Ruaha National Park,
Tanzania; panel g: GSD in Hoarusib River, Kunene Region, Namibia; panel h: GSD in Etosha
National Park, Namibia; panel i: GSD in Kruger National Park, South Africa; panels j, k, l: GSD
in Chobe National Park, Botswana; panel m: GSD in Hwange National Park, Zimbabwe; panel n:
GSD in Oregon Zoo, Oregon, USA; panel o: GSD in B. Bryan Preserve, California, USA.
31
Figure 1.2. (cont’d)
32
Figure 1.2. (cont’d)
33
Figure 1.3.
Variation in the severity of GSD in two distinct giraffe populations. Panels a. b, c: mild,
moderate and severe GSD in Rothschild’s giraffes (G. c. rothschildi) in Murchison Falls
National Park, Uganda and panels d, e, f: mild, moderate and severe GSD in Masai giraffe (G. c.
tippelskirchi) in Ruaha National Park, Tanzania.
34
Figure 1.4.
Variation in the anatomical location of GSD lesions. The x-axis represents the number of times
the GSD lesions were recorded in different study sites for a given anatomical location.
16
Number of times recorded
14
12
10
8
6
4
2
0
Limbs
Back
Neck
Chest
Head
Anatomical location on giraffe body
35
Entire body
Figure 1.5.
Secondary infections, characterized by inflammations, in giraffe populations in Ruaha National
Park, Tanzania.
36
Figure 1.6.
Manifestation of giraffe skin disease in a female Rothschild’s giraffe (G. c. rothschildi) before
(a) and after (b) washings using 1:50 dilute chlorhexidine solution in Paignton Zoo
Environmental Park, England.
37
Figure 1.7.
Unidentified skin lesions observed in wild and captive populations of giraffe. These lesions are
suspected to be related to GSD. Panel a: lesions on an Angolan giraffe (G. c. angolensis) in
Passage Valley, Central Kalahari Game Reserve in Botswana; panel b: giraffe ear disease on a
Masai giraffe (G. c. tippelskirchi) in Ruaha National Park, Tanzania; panel c: otitis on a Masai
giraffe (G. c. tippelskirchi) in Ruaha National Park, Tanzania; panel d: lesions on an Angolan
giraffe (G. c. angolensis) in the central part of Etosha National Park, Namibia; panels e, f:
blisters and lesions on the lower leg and foot of a Rothschild’s giraffe (G. c. rothschildi) in
Chester Zoo, England.
38
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39
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44
CHAPTER 2
EXAMINING DISEASE PREVALENCE FOR SPECIES OF CONSERVATION
CONCERN USING NON-INVASIVE SPATIAL CAPTURE-RECAPTURE
TECHNIQUES
Abstract
Non-invasive techniques have long been used to estimate wildlife population abundance and
density. However, recent technological breakthroughs have facilitated non-invasive estimation of
the proportion of animal populations with certain diseases. Giraffes (Giraffa camelopardalis) are
increasingly becoming recognized as a species of conservation concern with decreasing
population trajectories across their range in Africa. Diseases may be an important component
impacting giraffe population declines, and the emerging ‘Giraffe Skin Disease’ (GSD),
characterized by the appearance of wrinkled skin and alopecic lesions on the limbs, neck, and
chest of infected giraffe, may hinder movement causing increased susceptibility to predation. I
examined the prevalence of GSD in Tanzania’s Ruaha National Park over a 4-month period in
2015, using photographic capture-recapture surveys via road-based transects. I divided the study
area into 5 circuitous survey units, each approximately 100 km in length (x̅ = 99.22 km, SD =
3.72), and surveyed for giraffes for four months. From these surveys, I developed a database of
spatially-explicit giraffe photographs. I processed these photos for individual identification and
fitted spatial capture-recapture models to predict the spatial configuration of giraffe abundance
and GSD prevalence within the study area. My results indicated that >86% of the giraffe
population showed signs of GSD. I discuss the implications of this research for conservation of
threatened species with an emphasis on disease ecology and vulnerability to predations, and
more broadly, for wildlife conservation.
45
2.1.
Introduction
Recent technological and quantitative advancements have improved the accuracy and
expanded the scope of methods for estimating wildlife population parameters (Karanth et al.
2006; Royle et al. 2014). Non-invasive survey techniques can facilitate accurate estimation of
wildlife population abundance and density (Gompper et al., 2006), portray both species detection
and movement (Gerber et al., 2010; Thorn et al., 2011), and be used to develop basic ethograms
of animal behaviors (Young & Monfort, 2009). These non-invasive survey techniques, including
camera trapping, photographic surveys, and distance sampling have also enabled scientists to
quantify both mortality and recruitment rates in wildlife populations, even for rare and elusive
species (Marucco et al. 2009; Kéry et al., 2011). More recent developments have facilitated noninvasive estimation of disease prevalence (Ferreira & Funston, 2010; Langwig et al., 2012;
Liccioli et al., 2015). This research holds great promise for relating diseases to wildlife
population processes. In these ways, non-invasive survey techniques can inform the development
of progressive policies to conserve species of conservation concern (Gerber et al., 2010; Seimon
et al., 2013).
Non-invasive sampling is especially advantageous and cost-effective when certain
characteristics of individual animals can be easily observed and documented (e.g., using
photographs). These characteristics, which can be recognized and quantified via non-invasive
observation, allow scientists to obtain individual capture histories and estimate population
abundance with increased precision over large areas (Karanth et al., 2006; Bolger et al., 2012).
Spatial capture-recapture (SCR) techniques have proved effective in providing spatially-explicit
estimates of population abundance for species with unique pelage characteristics and coat
patterns (Royle et al. 2011). These models can also adjust for variation in animal encounter rates
46
due to individual characteristics that might affect behavior and estimate the proportions of these
the population that possesses these characteristics (e.g., Sollmann et al., 2011). Such spatiallyexplicit information could be immensely valuable for threatened species that are vulnerable to
diseases (Kolmstetter et al., 2000; Keawcharoen et al., 2004; Seimon et al., 2013).
Until recently, giraffes (Giraffa camelopardalis) have received little conservation
attention (Giraffe Conservation Foundation [GCF], 2013). Public perceptions that giraffes are
common, predicated (at least in part) by the regularity of giraffes in captive institutions, have
potentially masked the declining trends for wild-living giraffe populations. In reality, giraffe
populations have declined by ~40% in the last three decades (GCF, 2010, 2013; International
Giraffe Working Group, 2012), and the International Union for the Conservation of Nature
(IUCN) is currently assessing the species, which may shortly result in threatened species listing
on the IUCN Red List (J. Fennessy, pers. comm). Causal mechanisms associated with these
declines include habitat loss, poaching, and human encroachment (GCF, 2013). Giraffe
populations across Sub-Saharan Africa also seem to be increasingly affected by emerging
diseases (Karimuribo et al., 2011; Muneza et al. in review). Little is known of the prevalence and
potential impacts of emerging diseases on the conservation of giraffes.
While giraffes are prone to a number of well-known diseases including anthrax (Kaitho et
al., 2013), lumpy skin disease (Hunter & Wallace, 2001), giraffe ear disease (Karimuribo et al.,
2011), polyarthritis (Hammond et al., 2003), fibropapilloma infection (Karstad & Kaminjolo,
1978; van Dyk et al., 2011), and sarcoptic mange (Alasaad et al., 2012), there is an emerging
disease, generically referred to as Giraffe Skin Disease (GSD), for which only cursory
information exists (Muneza et al., in press). Characterized as a patchy skin infection, GSD
afflicts various parts of giraffe bodies. Giraffe skin disease lesions have been observed on the
47
necks and shoulders of giraffes in Uganda and Kenya; limbs, shoulders, and necks of giraffes in
Tanzania and Namibia; and upper body and necks in Botswana, Zimbabwe, and South Africa
(Muneza et al., in press). In the early stages of GSD, the skin appears to be wrinkled. Effected
area(s) can develop into chronic scabs that typically present with encrustations of dried or oozing
blood (Kalema, 1996; Epaphras et al., 2012; Brown & Fennessy, 2014, Muneza et al., in review).
It is possible that GSD also affects body condition as afflicted individuals have exhibited reduced
movements (e.g. standing in the same place for prolonged period of time), potentially affecting
their susceptibility to predation (Epaphras et al, 2012). However, these observations might only
apply to giraffes with severe GSD, as giraffes with moderate to mild GSD appear to move with a
relatively normal gait (Epaphras et al., 2012).
The occurrence, prevalence, and severity of GSD varies spatially. Tanzania’s Ruaha
National Park has the highest reported prevalence of GSD; >79% of the animals observed during
a 3-day survey exhibited signs of GSD infection (Epaphras et al., 2012), and this prevalence was
33% higher than reported for any other giraffe population in the country (Muneza et al., in
press). Importantly however, this metric was calculated based on the proportion of animals
observed, rather than the proportion of the population. Disease prevalence among animals
observed alone does not explicitly consider spatio-temporal correlation in the distribution of
diseased animals. For instance, there could be clustering or dispersion in the spatial patterns of
the disease. Failure to consider these factors can bias the estimation of the resultant metrics,
potentially over- or under-estimating the prevalence of a disease, given that the animals would
not be drawn from independent samples. Thus, there is a need to assess disease prevalence at the
population level, with consideration of these spatial relationships. However, assessing
population-level parameters requires that members of the population can be individually
48
recognized. The unique coat patterns of giraffes facilitate such estimations via non-invasive
research techniques. Spatially-explicit estimates of disease prevalence could be valuable for
wildlife populations that are vulnerable to diseases (Kolmstetter et al., 2000; Keawcharoen et al.,
2004; Seimon et al., 2013). Here, I estimate the prevalence of GSD in the giraffe population of
Ruaha National Park. I conducted non-invasive surveys to individually identify giraffes (based
on pelage characteristics) and fit SCR models. I used these models to predict the proportion of
the giraffe population exhibiting GSD. I discuss the implications of this research for giraffe
conservation, giraffe-carnivore interactions, and disease ecology of species of conservation
concern more broadly.
2.2.
Methods
2.2.1. Study area
Ruaha National Park is the largest national park in Tanzania (20,226 km 2) and is located
in the south-central part of the country (7°30’00”S, 35°00’00”E), with its highest point 1,886 m
above sea level (Fig. 2.1; NBS, 2013). Ruaha National Park has a generally hot and dry tropical
climate and is a priority for carnivore conservation in Africa, home to over 10% of the world’s
lions (Panthera leo; Riggio et al., 2012; Abade et al., 2014), and important populations of
leopards (Panthera pardus), spotted hyaenas (Crocuta crocuta), African wild dogs (Lycaon
pictus), and cheetahs (Acinonyx jubatus). These carnivores persist in this landscape by hunting a
variety of prey species including zebras (Equus quagga), elands (Taurotragus oryx), impala
(Aepyceros melampus) and giraffe (G. c. tippelskirchi; IUCN, 2007). The road network covers
only a small proportion (roughly 12%) of the park (Fig. 2.1). The majority of the park is roadless and mostly inaccessible to vehicles.
49
2.2.2. Vehicle-based photographic surveys
I conducted a series of vehicle-based photographic surveys for giraffes in Ruaha National
Park between May and August 2015. I divided the existing road network in the park and
surrounding village and wildlife management areas into 5 circuitous survey units of ~100 km in
length (𝑥̅ = 99.22 km, SD = 3.72; Fig. 2.1). I surveyed each of these 5 survey units at least 10
times during the study and randomized both the start day and the direction traveled for each
survey (Table 1).
I positioned observers on both sides of the vehicle to detect giraffes. I maintained a
consistent speed (approximately 20 km/hour) and scanned the environment on both sides of the
road. Detection of giraffes at this speed was high given that 1) giraffes are the tallest animals on
earth, 2) vegetation in Ruaha National Park is lower than giraffe height and 3) I recorded giraffes
observed with a 200m transect width. Hence I assumed no observational error in giraffe
detection. When giraffes were observed, I recorded sex, age class (calf, subadult or adult), herd
size, presence and severity of GSD, evidence of previous lion predation attempts (i.e. claw
marks, missing tails, and bite marks), and took right-side photographs of each animal using a
Nikon D300S camera with an auto-focus-S DX NIKKOR 70-300mm f/3.5-5.6 ED VR lens. I
connected the Nikon camera to a Garmin GPSMap 78Sc GPS unit so that each image was georeferenced. I assessed the distance of each animal from our vehicle using a Nikon 8397
ACCULON Laser Rangefinder. I used the right-side photographs to maintain consistency in my
efforts to identify individuals via the application of Wild-ID software (see details below). I
recorded the severity of GSD in an individual giraffe based on the categories used by Kalema
(1996) and Epaphras et al. (2012), which included none (no visible signs of the disease), mild
(small skin nodules of ~2-3cm in diameter with raised hair), moderate (medium sized patch of
50
alopecic lesions of 10-16cm in diameter), and severe (large-sized lesions >16cm in diameter,
skin wrinkles, scabs, scales, cracks with raw fissures).
Following Bolger et al. (2012), I used digital images of the right side of giraffes to obtain
capture histories of individuals observed in the population. I cropped the images that clearly
depicted the area of interest (I discarded photos that were taken from an acute angle and photos
in which vegetation obstructed the side of the animal). I then used Wild-ID to extract the
distinctive pattern of each individual giraffe by matching each image to my database of all other
images recorded (Fig. 2.2). Using Scale Invariant Feature Transform (SIFT) algorithms (Lowe,
2004; Bolger et al., 2012), Wild-ID characterized giraffe coat patterns in the images and assigned
similarity scores of the images ranging from 0.000 to 0.9999. The top-ranked image was selected
as the matching pair. I further inspected each pair visually before proceeding so as to avoid false
acceptance. When in doubt, I inspected the top 5-ranked images and selected the photo with the
highest ranking that could be visually matched. The results from the photographic SCR analysis
via application of Wild-ID yielded the encounter histories of giraffes across my 4-month study
period.
2.2.3. Spatial Capture Recapture
I estimated giraffe population parameters using SCR with a search-encounter design
(Royle et al., 2014). I divided the survey region, defined by the accessible road network, into
discrete grid cells (1 km × 1 km) and considered any grid cells overlapping a survey unit (road
transect) as “traps” within which a giraffe could be encountered. I assumed that each individual i
had an associated activity center si describing the coordinates around which individual
movement occurred (Borchers & Efford, 2008; Royle & Young, 2008). The activity centers were
distributed uniformly as a homogeneous point process as si ~ Uniform(S), where S represents a
51
region encompassing the survey units buffered by 7.5 km (as an estimate of the distance covered
by an individual giraffe in one day), to include the activity centers of all individuals that may
have been encountered. The number of encounters for individual i in surveyed grid cell j was
considered a Poisson random variable with mean encounter rate λij which varied by individual
and grid cell. Importantly, the encounter rate decreased with increasing distance dij between the
activity center for individual i and the location of grid cell j, such that:
λ ij  λ 0ij  exp  dij2 2σi2 
Here, λ0ij is the encounter rate when grid cell j overlaps the activity center for individual i such
that dij  0, while σi is the scale parameter of the half-normal detection function, controlling the
decay in encounter rate with increasing distance.
As indicated by the subscripts, λ0ij and σi were allowed to vary by individual attributes
that I hypothesized might influence individual movement including sex, age class (adult vs.
subadult), and the number of legs with severe patches of GSD (0, 1, 2+). Calves were eliminated
from consideration because their movements depended upon their mother, thus violating the
assumption of individual independence necessary for SCR models (Royle et al. 2014). I also did
not consider the number of legs with mild or moderate GSD lesions, assuming severe lesions
would have the greatest effect on behavior. I modeled the effects of individual attributes using a
log-link for both parameters, such that log(λ0ij)  Xiα and log(σi)  Xiδ, where Xi is a vector from
the design matrix of individual attributes while α and δ indicate vectors of regression coefficients
for each parameter. The regression coefficients involved 2 effects terms and an interaction for
the binary categories (i.e., sex, age class) and a linear effect for number of severe GSD legs. In
addition to the individual attributes, I included an offset term on the encounter rate to adjust for
52
the total hours spent surveying a grid cell, calculated as the total survey duration scaled by linear
length of overlapping survey units.
The population size, N, was determined by the number of activity centers within S. I used
data augmentation to estimate N (Royle & Dorazio, 2012) whereby the encounter data for the n
observed individuals were augmented with a large number (M – n) of “all-zero” encounter
histories, a portion of which correspond to true members of the population that were never
encountered. Each individual was assigned a partially latent membership indicator, zi, which
takes the value of 1 for true members of the population and 0 otherwise; the value of zi is known
to be 1 for all n observed individuals and treated as missing data for the M – n individuals. I
considered zi a Bernoulli random variable and estimated the proportion of M with zi  1 as:
zi ~ Bernoulli(ψ)
Population size was then determined by the sum of the zi or equivalently, ψ × M. I set M to a
value large enough to prevent truncation of the posterior distribution for N. The estimate of
density, D, was derived by dividing N with the area of S.
The individual attributes of sex, age class, and number of severe GSD legs were unknown
for the M – n unobserved individuals and were treated as missing data similar to the membership
indicators. Importantly, if encounter rates differed by individual attributes then the observed
proportions of each would be biased; I adjusted for potential bias by explicitly estimating the true
proportions for each attribute. For the binary categories of sex and age class, I estimated the
proportion of males (ψmale) and the proportion of subadults (ψsubad). I treated number of severe
GSD legs as a zero-inflated multinomial random variable with ψ GSD representing the probability
53
of an individual having any signs of GSD, and φk representing the conditional probability of
having k  0, 1, or 2+ severe legs. For individuals without GSD, Pr(k  0)  1.
I used a Bayesian approach to model estimation using Markov chain Monte Carlo
(MCMC) methods in JAGS (Plummer, 2003) with the jagsUI package (Kellner, 2014) in R (R
Core Team, 2015). Model code written in the BUGS language (Lunn et al., 2000) is provided in
Appendix 1. I used vague prior distributions for all model parameters including Uniform(0, 1)
for all probabilities; Uniform(–10, 10) for log-scale intercepts α0 and δ0; and Normal(0, 100) for
all other regression coefficients (i.e., α1–4 and δ1–4 ). I fit 3 chains of 10,000 iterations with a
1,000 iteration burn-in, leaving 27,000 values forming the posterior distribution for each
parameter. Model convergence was assessed using trace plots and examination of the R-hat
statistic (Gelman et al., 2013); I ensured an R-hat value <1.1 for all model parameters. I report
posterior median values with 95% credible intervals for model parameters regression coefficients
with 95% credible intervals that did not overlap zero as strong evidence for an effect.
2.3.
Results
I recorded 336 sightings of one or more giraffes in Ruaha National Park. I observed 1,333
giraffes during my surveys. I identified 753 of these animals as adult females, 288 adult males,
77 subadult females, 70 subadult males, and 113 calves. There were 32 giraffes for which I could
not identify sex because of blocking vegetation and, as such, I excluded these animals from
consideration in this analysis. On average, the number of giraffes in a herd was 3.94 (range 1 –
36). From these surveys I collected 2,129 photographs that satisfied criteria for inclusion in the
SCR analysis (i.e., they were suitable for examination in Wild-ID software). There were only 10
cases in which I failed to capture useable images of giraffes. These encounters occurred when a
54
giraffe was running away from our location and into thick vegetation. Via post-processing of
these images in Wild-ID, I identified 622 individual giraffes. Among these giraffes, 333 were
adult females, 160 adult males, 38 subadult females, 32 subadult males, and 59 calves. I modeled
the capture histories of 563 adult and subadult individual giraffes.
Model results indicated an adult/subadult population density of 0.55 [0.49, 0.62] giraffes
per km2 (Table 2.2). The population had lower proportions of males (ψmale  0.35 [0.30, 0.42])
and subadults (ψsubad  0.13 [0.09, 0.18]) and a high proportion of individuals with GSD (ψGSD 
0.86 [0.83, 0.89]). The occurrence of GSD infection for individual giraffes did not change during
my study, so I assumed that there was no error in detecting visible GSD. However, I could not
determine the occurrence of GSD in 0.1% (n=5) of the population because the legs of the
animals were not visible. Among the 478 giraffes that exhibited signs of GSD, 309 (64%) were
females, 145 (30%) males, 14 (3%) subadult females, and 8 (2%) subadult males. The proportion
of individuals having 0, 1, or 2+ legs with severe lesions was mostly even (Table 2.2), and
number of legs with severe lesions did not have strong effects on individual encounter rate (α4 
–0.04 [–0.19, 0.24]) or the scale parameter of movement (δ4  –0.07 [–0.16, 0.03]), though 93%
of the posterior distribution for the latter was negative. Movement was greatest for subadult
males (δ3  0.61 [0.14, 0.96]) and lowest for subadult females (δ2  –0.36 [–0.56, –0.01]).
Realized giraffe density was highest in the north eastern portion of the sampling area, notably
along the Mdonya and Serengeti Ndogo survey routes (Fig. 2.3). Realized prevalence of GSD
was lowest in the southwest portion of the sampling area, where 80% of individuals were
afflicted, compared to other areas with >90% prevalence.
55
2.4.
Discussion
Prior research has identified that Ruaha National Park, Tanzania has a population of
giraffes with the highest rates of GSD recorded in Africa (Epaphras et al., 2012). This study
found that 79.8% of animals observed showed signs of GSD. Given that this study occurred over
a short 3-day survey, and did not assess the prevalence of GSD at the population-level, there was
a need to assess whether almost 80% of this population could actually be afflicted with this
disease. To further substantiate the prevalence of GSD in Ruaha, my analysis revealed that an
even higher proportion of the population is affected by GSD. I found a minimum of 86% of the
giraffe population in Ruaha National Park had visible signs of GSD, which is over 6% higher
than reported by Epaphras et al. (2012). This estimate of GSD prevalence is the highest recorded
anywhere in Africa, corroborating that Ruaha National Park is indeed a hotspot for GSD.
Research dedicated to understanding the epidemiology and ecology of GSD, and its possible
threats to giraffe conservation, should focus on Ruaha National Park.
With a density of 0.53 giraffes per km2 (Table 2.2), Ruaha National Park remains one of
the most important areas for giraffe conservation (Stoner et al., 2007). Only Serengeti National
Park in Tanzania has more giraffes (Strauss, 2014). Tarangire National Park, Tanzania also has a
high number of giraffes, with the second highest recorded prevalence of GSD in Africa (63%;
Lee & Bond, 2013; Lee, 2015). I estimated that there were 1,736 giraffes in study area S (Table
2), with no clear links between giraffe abundance or density and the occurrence or prevalence of
GSD. Infectious diseases in wildlife can spread rapidly when animals occur in high abundances
or aggregate in close proximity (Daszak et al., 2000; Gortázar et al., 2006). It is not yet known if
GSD is infectious, how it might spread among giraffes, whether it is communicable to other
organisms, or even the etiological agent that is present (Muneza et al., in press). Thus, this is an
56
area where veterinarians, disease ecologists, conservationists, and managers must collaborate to
fully assess the potential effects of GSD on giraffe populations.
I detected evident spatial variation in giraffe density within Ruaha National Park, with
giraffe the highest densities occurring in the northern and north-eastern portions. These areas
(Mdonya and Serengeti Ndogo survey units) provide important sources of water for wildlife
(Epaphras et al., 2007), especially during the dry season. It remains unknown whether GSD is a
waterborne disease that affects adult giraffes, which have been observed drinking in large
numbers near both natural and artificial waterholes (Epaphras et al., 2007). It also remains
unclear whether this disease is communicable to other species, since I did not observe any others
animals in Ruaha that have a disease that manifests in a comparable way to GSD on giraffes. My
sampling period coincided with the beginning of the dry season and encounter rates of giraffe
were higher near water sources. In this way, my density estimates reflect dry season estimates.
Whether seasonality influences GSD epidemiology requires additional investigations.
Additionally, in some areas, notably the Jongomero and Nyamasomba survey units, the presence
of dense miombo woodlands, which is suitable habitat for biting insects (tsetse flies (Glossina
palpalis); Cecchi et al., 2008), could have affected the spatial distribution of giraffe populations.
The only portion in the Jongomero survey unit with a high giraffe density was an open area with
a semi-permanent source of water and presumably a lower density of biting insects. Despite the
high density of giraffes in Jongomero, the prevalence of GSD was lower than compared to the
northern and eastern sides of the park. Studying the link between giraffe density and prevalence
of GSD could be another area of interest for further research opportunities.
While almost all giraffes with GSD had lesions on their limbs, I failed to document any
differences in movements based on the severity of the infection. Previous studies have observed
57
that giraffes with severe lesions have reduced movement (Epaphras et al., 2012; Muneza et al., in
press). Affected giraffes have been reported to stand in one spot for extended periods of time or
move carefully (Epaphras et al., 2012; Muneza et al. in press). My findings herein indicate that
the number of legs with severe GSD lesions did not have a strong influence on the scale
parameter of movement or the encounter rate of affected individual giraffes. Specifically, the
scale parameter of movement was not significantly related to severity of the GSD infection,
though the posterior distribution of the effect was largely negative. I only observed inhibited
movements for affected animals with severe lesions that also had poor body condition and claw
or bite marks indicating predation attempts by lions. To my knowledge, there has been no link
established between GSD and body condition of affected giraffe, which may lead to increased
vulnerability to lion predation (Hirst, 1969).
However, I did detect evident variation in movement parameters by sex of giraffes. My
results illustrate that males, especially subadult males, moved more than females (Table 2.2).
Subadult female giraffes moved the least, consistent with the average movement patterns of
giraffes observed in other populations (Fennessy, 2009; Bercovitch & Berry, 2013; Strauss,
2014). Male giraffes move further than females in search of mates, to forage or to establish
dominance (Fennessy, 2009). These differences in movements affected the probability that an
individual would be encountered and identify the ability of SCR models to analytically account
for such differences in behavior (Sollmann et al. 2011). Had the severity of lesions also
significantly affected movement, standard population estimation methods that do not account for
spatial variation in encounter of individuals due to location and movement would produce biased
results. My results highlight the strength of SCR as a framework for estimating population size,
or density, without having to define the effective trapping or observation area (Royle et al. 2014),
58
which can otherwise complicate and bias population estimation at large scales (Soisalo et al.
2006; Foster et al. 2012).
In conclusion, this study has shown that data from non-invasive surveys can be used in
SCR models to estimate the proportion of a population affected by a visible disease. The SCR
models also incorporated population parameters such as sex and age class, movement, and
encounter rate, which may be linked to the prevalence of the disease. This is particularly useful
for studies on wildlife diseases in species of conservation concern whereby invasive survey
methods may be costly or risky to animals. For instance, there are several areas in sub-Saharan
Africa where GSD has been observed but the proportion of population affected has not been
assessed or has been assumed to be low (Muneza et al., in press). Researchers and
conservationists can use SCR models to better examine the variation in parameters associated
with these populations (such as movement, sex, births/deaths) and GSD, while incorporating
broad spatial and temporal dimensions of the population in such areas. This flexibility shows the
usefulness of non-invasive survey techniques, which can be used for a wide range of wildlife
species, providing that certain characteristics make individuals recognizable. For instance,
photographic mark-recapture has been used to accurately identify amphibians (Bendik et al.,
2013), which are threatened by both diseases (Piotrowski et al., 2004) and climate change
(Wake, 2007). With the ability to identify individuals, researchers can gather more data on the
ecology and population dynamics of declining, rare or elusive species using SCR models, which
will help improve the study of disease ecology, inform conservation efforts, and guide the
implementation of management.
59
Acknowledgements
My thanks go to WildCRU at the University of Oxford and the RECaP Laboratory at Michigan
State University (MSU) for guidance in preparation of this manuscript. I extend my gratitude to
the MasterCard Foundation Scholars Program at MSU, the Giraffe Conservation Foundation, the
Leiden Conservation Foundation, and the American Society of Mammologists for their generous
support of this research. I thank S. Lipenga, M. Kimaro, N. Zuberi, A. Msago, J. Chambulila, U.
Mgogo, G. Kimathi, R. Lipenga, S. Enock, G. Sedoyeka, B. Lawa, D. Bora, and all the staff at
Ruaha Carnivore Project and Ruaha Lion Guardians for their incredible support and participation
in data collection.
60
APPENDIX
61
APPENDIX
Table 2.1. List and direction of 2015 survey routes in Ruaha National Park, Tanzania. The
direction was determined randomly from the start point on a given survey route and
the day of survey is counted from the first day a survey route was successfully
completed.
Jongomero
Serengeti Ndogo
Nyamasomba
Mdonya
WMA
Day
Direction Day
Direction Day
Direction Day
Direction Day
Direction
1
West
2
West
3
West
4
West
9
East
6
West
5
West
6
East
8
East
11
West
10
East
7
East
9
West
10
East
17
East
14
East
12
East
14
West
13
West
19
West
18
West
15*
West
20
East
16
West
22
East
21
East
17*
East
21
West
20
East
25
West
24
West
19
West
24
East
23
West
26
East
28
West
22*
West
28
East
27
East
31
East
29
East
23
West
29
West
30
East
32
West
33
East
27
East
34
West
33
West
34
West
30
East
31
East
32
West
* Vehicle broke down and route was not completed
62
Table 2.2. Parameter estimates (median and 95% credible interval) from the spatial capturerecapture model of adult and subadult giraffes in Ruaha National Park, Tanzania in
2015. Parameters include probabilities for individual attributes such as population
membership (ψ), sex (ψmale), age class (ψsubad), signs of GSD (ψGSD), and number of
legs with severe lesions (φk); log-linear regression coefficients for the encounter rate
(α) and the scale parameter of the half-normal detection function (δ); and derived
parameters of population size (N) and density (D) per km2.
Parameter
Effect
Median
95% CRI
Ψ
0.77
[0.68, 0.86]
ψmale
0.35
[0.30, 0.42]
ψsubad
0.13
[0.09, 0.18]
ψGSD
0.86
[0.83, 0.89]
φk=0
0.33
[0.38, 0.28]
φk=1
0.37
[0.37, 0.35]
φk=2+
0.31
[0.24, 0.37]
α0
–1.72
[–1.99, –1.45]
–0.45
[–0.83, –0.08]
0.48
[–0.15, 1.10]
α1
male
α2
subadult
α3
male × subadult
–0.62
[–1.53, 0.29]
α4
# severe legs
–0.04
[–0.19, 0.24]
0.91
[0.79, 1.02]
0.13
[–0.02, 0.32]
–0.36
[–0.56, –0.01]
δ0
δ1
male
δ2
subadult
δ3
male × subadult
δ4
# severe legs
0.61
[0.14, 0.96]
–0.07
[–0.16, 0.03]
N
1819
[1614, 2040]
D
0.55
[0.49, 0.62]
63
Figure 2.1.
Survey routes in the sampling area in Ruaha National Park, Tanzania. The map only shows the
road network that was used for the survey and each circuit is represented by a different color.
64
Figure 2.2.
User interface of Wild-ID software showing right-side image of interest (top left and bottom
left), active window (bottom right) and potential matches (top row and arranged from right to left
in a descending order of rank score).
65
Figure 2.3.
Predictive map of realized giraffe density and GSD incidence in the survey area of Ruaha
National Park, Tanzania in 2015. Using SCR models, the plot shows potential areas of GSD
hotspot and higher centers of activity. Grid cell resolution was 2 km × 2 km.
66
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CONCLUSION
Giraffes are among the most understudied megafauna. Despite the important roles they
play in the ecosystem, there is limited research on free-ranging giraffe populations in subSaharan Africa (GCF, 2013). This study focused on a wildlife disease that was first described in
1996 but remained largely unstudied until recently. In chapter 1, I assessed available literature to
assess the regional variation in the manifestation, prevalence and severity of GSD. With these
data, I showed areas that may be hotspots of the disease, notably East Africa, and provided
baseline data that can be used in mitigation efforts of GSD. There are vast areas of sub-Saharan
Africa still without any information on GSD and this study lays the foundation for future studies
that aim to better understand the direct and indirect effects of GSD on the vital rates of giraffe
populations both in the wild and in captivity. In chapter 2, I demonstrated how spatial capturerecapture models can be used to estimate the prevalence of a disease at the population-level for a
species that is of growing conservation concern. I also discussed how these techniques are not
species-specific and are, rather, applicable to any wildlife species that may be individuallyrecognizable and suffering from a disease that manifests on the exterior of the animals’ body.
With emerging infectious diseases of wildlife being recognized as a threat to mammal
populations, this study illustrates the use of non-invasive techniques in examining disease
prevalence to better understand the direct and indirect effects of infections in wildlife
populations.
The strengths of this study are that 1) it is the most current database of known cases of
GSD in wild and captive giraffe populations, and shows that GSD is prevalent in more areas in
sub-Saharan Africa than initially thought; 2) it demonstrates how the results of disease-modified
spatial capture-recapture models can be used to develop a spatial prediction across a study area
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to identify hotspots in the spatial distribution of a disease. The limitations of this study are that 1)
the current categories of severity of GSD that are widely used are based on arbitrary descriptions
(Kalema, 1996; Epaphras et al., 2012); 2) there is very limited quantitative data on the
prevalence of GSD in wild giraffe and the available data were not collected in a uniform manner
by the researchers and veterinarians in different study areas across Africa to allow the use of
statistical analyses; 3) the estimates for Ruaha National Park in chapter 2 reflect the estimations
for the dry season. Thus, I recommend that future studies 1) identify a standard protocol of
quantifying severity of GSD; 2) assess the status of GSD in areas where the disease has been
reported; 3) isolate and characterize the etiological agent of the disease; 4) examine the effect of
GSD on giraffe-lion interactions in Ruaha National Park, which has the highest prevalence of the
disease and giraffe appear to be a preferred prey of lions; 5) provide giraffe health guidelines in
light of the emergence of GSD. These research opportunities would advance giraffe conservation
and more broadly, wildlife conservation practices.
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REFERENCES
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REFERENCES
1) Epaphras, A. M., E. D. Karimuribo, G. D. Mpanduji and E. G. Meing’ataki. 2012. Prevalence,
disease description and epidemiological factors of a novel skin disease in Giraffes (Giraffa
Camelopardalis) in Ruaha National Park, Tanzania. Research Opinions in Animal and
Veterinary Sciences 2(1):60 – 65
2) Giraffe Conservation Foundation. 2013. Africa’s Giraffe (Giraffa camelopardalis): A
conservation guide. Black Eagle Media. Western Cape, South Africa.
3) Kalema, G. 1996. Investigation of a skin disease in giraffe in Murchison Falls National Park.
Uganda National Parks. Kampala, Uganda.
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