Mapping the Spatial Configuration and Severity of Giraffe Skin Disease in Ruaha National Park, Tanzania

Home , Angolan giraffe, Gambella National Park, Mikumi National Park, Ruaha National Park

MAPPING THE SPATIAL CONFIGURATION AND SEVERITY OF GIRAFFE SKIN DISEASE IN RUAHA NATIONAL PARK, TANZANIA

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

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.

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

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 capture- recapture 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

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 stem- boring 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 non- invasive survey techniques to estimate the prevalence of a disease for wildlife conservation.

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

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.

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

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 peer- reviewed 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.

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),

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 2-

3cm in diameter with raised hair, that later become larger round or oval alopecic patches of 10-

16cm 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).

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.

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,

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 km2 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 free- ranging 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.

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.

APPENDIX

Table 1.1. List of sources that reference descriptions of skin diseases in populations of wild giraffe.

Study Study area Country Disease Reference Type of period literature 1970 Kruger National LSD Young, 1970 Peer-reviewed South Park (lab research paper Africa experiment) 1976 Kiboko Papillomavirus Karstad and Peer-reviewed Kenya infection Kaminjolo, research paper 1978 1988 NAa Regional LSD Woods, 1988 Review paper 1991 NAa Lumpy Skin Davies, 1991 Review paper Regional Disease 1996 Murchison Falls Giraffe Skin Kalema, 1996 Unpublished Uganda National Park Disease report 2001 NAa Lumpy Skin Hunter and Review paper Regional Disease Wallace, 2001 2004 NAa Lumpy Skin Coetzer and Book chapter Regional Disease Tustin, 2004 extract 2007- Kruger National South Papillomavirus van Dyk et al., Peer-reviewed 2008 Park Africa infection 2011 research paper 2011 NA Giraffe Skin Karimuribo et Review paper Tanzania Disease al., 2011 2011 Ruaha National Giraffe Skin Mpanduji et al. Unpublished Tanzania Park Disease 2011 report 2012 Ruaha National Giraffe Skin Anon, 2012 Call for Tanzania Park Disease proposals 2012 Ruaha National Giraffe Skin Epaphras et Peer-reviewed Tanzania Park Disease al., 2012 research paper 2012 – Tarangire Tanzania Giraffe Skin Lee and Bond, Unpublished Present National Park, Disease 2012 report Manyara National Park, Manyara Ranch Conservancy, Ngorongoro Conservation Area, Serengeti National Park, Arusha National Park

Table 1.1. (cont’d)

Study Study area Country Disease Reference Type of period literature 2013 Ruaha National Giraffe Skin WCS, 2013 Unpublished Tanzania Park Disease report 2014 Murchison Falls Giraffe Skin Brown and Unpublished National Park Uganda Disease Fennessy, report 2014 2014 Ruaha National Giraffe Skin Epaphras et Unpublished Tanzania Park Disease al., 2014 report *Paper analyzes studies conducted in multiple areas and aggregates findings in a systematic review paper.

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 Type of Location of lesions skin disorder Atherstone Nature Reservea South Africa LSD NA Chobe National Parkb Botswana GSD Upper body Entabeni Game Reservea South Africa LSD NA Etosha National Parka Namibia GSD Limbs Hoarusib River, Kunene Regiona Namibia GSD Limbs Hwange National Parkb Zimbabwe LSD and Upper body* GSD Ithala National Parkb South Africa LSD NA Kruger National Parkb South Africa GSD Upper body Lake Nakuru National Parkc Kenya GSD Limbs Manyara Ranch Conservancyd Tanzania GSD Limbs Murchison Falls National Parkc Uganda GSD Neck Ruaha National Parkd Tanzania GSD Limbs, neck Selous Game Reserved Tanzania GSD Limbs Serengeti National Parkd Tanzania GSD Limbs Soysambu Conservancyc Kenya GSD Limbs Tarangire National Parkd Tanzania GSD Limbs Banham Zood England GSD Limbs Bronx Zooc USA LSD NA Columbus Zoo and Aquariumd USA GSD Limbs Flamingo Landc England LSD NA Great Plains Zooe USA GSD Limbs Jacksonville Zoo and Gardense USA GSD Limbs, testicles, inner thigh, upper body La Reserva del Castillo de las Guardase Spain LSD NA Oregon Zooe USA GSD Limbs Paignton Zoo Environmental Parkc England GSD Limbs Parc de Beauvale France GSD Head Parco Natura Viva Garda Zoological Parkc Italy GSD Upper body Royal Zoological Society of Antwerpf Belgium GSD Upper body Safaripark Beekse Bergenc Netherlands GSD Entire body

*Refers to location of GSD lesions. For this study, I did not include the location of lumpy skin disease (LSD) lesions. aCape giraffe (G. c. giraffa) bAngolan giraffe (G. c. angolensis) cRothschild’s giraffe (G. c. rothschildi) dMasai giraffe (G. c. tippelskirchi) eReticulated giraffe (G. c. reticulata) fKordofan giraffe (G. C. antiquorum)

Table 1.3. Fungal species identified by Epaphras et al. (2014) that are suspected to be involved in the pathology of giraffe skin disease.

Fungal species name Auerobasidium pullulons Epicoccum sorghum Auerobasidium spp. Exsorohilum rostratum Aspergillus niger Fennellia nivea Aspergillus fruticulosus Fusarium equiseta Aspergillus multicolor Penicillium citrinum Aspergillus sydrowii Penicillium commune* Aspergillus versilor Penicillium griseofulvum† Cochliobolus lunatus* Phoma spp. Emericella omanensis

* Indicates fungal species that are also found in healthy giraffe.

† Indicates fungal species with anti-inflammation properties.

Table 1.4. Areas where signs of GSD have been assessed but not been detected in the local giraffe population. Location Country Giraffe subspecies Amboseli National Park Kenya Masai giraffe (G. c. tippelskirchi) Arusha National Park Tanzania Masai giraffe (G. c. tippelskirchi) Gambella National Park Ethiopia Nubian giraffe (G. c. Camelopardalis) Garamba National Park Democratic Kordofan giraffe (G. C. Republic of Congo antiquorum) Garden Route (Western Cape) South Africa Cape giraffe (G. c. giraffa) Laikipia and Samburu Kenya Reticulated giraffe (G. c. landscape reticulata) Lake Manyara National Park Tanzania Masai giraffe (G. c. tippelskirchi) Nairobi National Park Kenya Masai giraffe (G. c. tippelskirchi) Ngorongoro Conservation Tanzania Masai giraffe (G. c. tippelskirchi) Area Sioma Ngwezi National Park Zambia Thornicroft’s giraffe (G. c. antiquorum) Tama Wildlife Reserve Ethiopia Reticulated giraffe (G. c. reticulata) Tsavo West National Park Kenya Masai giraffe (G. c. tippelskirchi)

Figure 1.1. Distribution of giraffe (Giraffa camelopardalis) subspecies and giraffe skin disease in Sub- Saharan Africa.

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.

Figure 1.2. (cont’d)

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.

Number recorded of times Number 4

0 Limbs Back Neck Chest Head Entire body Anatomical location on giraffe body

Figure 1.5.

Secondary infections, characterized by inflammations, in giraffe populations in Ruaha National Park, Tanzania.

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.

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.

REFERENCES

1) Anon., 2012. Research study needed for giraffe skin disease in Ruaha National Park, Tanzania. Giraffa, 6:24.

2) Bercovitch, F. B., Berry, P. S. M., 2012. Herd composition, kinship and fission – fusion social dynamics among wild giraffe. African Journal of Ecology, 51 (2):206 – 216.

3) Blehert, D. S., Hicks, A. C., Behr, M., Meteyer, C. U., Berlowski-Zier, B. M., Buckles, E. L., Coleman, J. T. H., Darling, S. R., Gargas, A., Niver, R., Okoniewski, J. C., Rudd, R. J., Stone, W. B., 2009. Bat White-Nose Syndrome: An Emerging Fungal Pathogen? Science, 323:227

4) Bock, F., Fennessy, J., Bidon, T., Tutchings, A., Marais, A., Deacon, F., Janke, A., 2014. Mitochondrial sequences reveal a clear separation between Angolan and South African giraffe along a cryptic rift valley. BMC Evolutionary Biology, 14:219 – 230.

5) Boone, R. B., Thirgood, S. J., Hopcraft, J. G. C., 2006. Serengeti Wildebeest Migratory Patterns Modeled From Rainfall and New Vegetation Growth. Ecology. 87 (8):1987 – 1994.

6) Brenneman, R. A., Bagine, R. K., Brown, D. M., Ndetei, R., Louis Jr., E. E., 2009. Implications of closed ecosystem conservation management: the decline of Rothschild’s giraffe (Giraffa camelopardalis rothschildi) in Lake Nakuru National Park, Kenya. African Journal of Ecology, 47:711 – 719.

7) Brown, M. B., Fennessy, J., 2014. A preliminary assessment of Rothschild’s giraffe in Uganda. Giraffe Conservation Foundation. Unpublished report.

8) Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., Orme, C. D. L., Purvis, A., Multiple Causes of High Extinction Risk in Large Mammal Species. Science, 309 (5738):1239 – 1241.

9) Carter, K. D., Seddon, J. M., Frère, C. H., Carter, J. K., Goldizen, A. W., 2013. Fission – fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and individual social preferences. Animal Behaviour, 85 (2):385 – 394. DOI:10.1016/j.anbehav.2012.11.011

10) Ceballos, G., Ehrlich, P. R., Soberón, J., Salazar, I., Fay, J. P., 2005. Global Mammal Conservation: What Must We Manage? Science, 309 (5734):603 – 607.

11) Coetzer, J. A. W., Tustin, R. C., 2004. Infectious diseases of livestock. Cape Town, Oxford University Press Southern Africa. ISBN: 019578202X

12) Craigie, I. D., Baillie, J. E. M., Balmford, A., Carbone, C., Collen, B., Green, R. E., Hutton, J. M., 2010. Large mammal population declines in Africa’s protected areas. Biological Conservation, 143:2221 – 2228.

13) Dagg, A. I., 2014. Giraffe: Biology, Behaviour and Conservation. New York, Cambridge University Press. ISBN 978-1-107-03486-0.

14) Davies, F. G., 1991. Lumpy skin disease of cattle: a growing problem in Africa and the Near East. World Animal Review, 68 (3), 37 – 42.

15) Deem, S. L., Spelman, L. H., Yates, R. A., Montali, R. J., 2000. Canine distemper in terrestrial carnivores: A review. Journal of Zoo and Wildlife Medicine, 31 (4):441 – 451

16) Dodson, B., 2015. World Giraffe Day – A Different Perspective. Giraffid, 9 (2):4 – 7.

17) Epaphras, A. M., Karimuribo, E. D., Mpanduji G. D., Meing’ataki, E. G., 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.

18) Epaphras, A. M., Mwamengele, G. L., Misinzo, G., Mngumi, B. E., 2014. Investigation report on Giraffe Skin Disease in Ruaha National Park. Tanzania National Parks. Unpublished.

19) Estes, R. D., Atwood, J. L., Estes, A. B., 2006. Downward trends in Ngorongoro Crater ungulate populations 1986 – 2005: Conservation concerns and the need for ecological research. Biological Conservation, 131 (1):106 – 120. DOI: 10.1016/j.biocon.2006.02.009

20) Fennessy, J., 2004. Ecology of desert-dwelling giraffe Giraffa camelopardalis angolensis in northwestern Namibia. University of Sydney, Australia, PhD thesis.

21) Fennessy, J., Bock, F., Tutchings, A., Brenneman, R., Janke, A., 2013. Mitochondrial DNA analyses show that Zambia’s South Luangwa Valley giraffe (Giraffa camelopardalis thornicrofti) are genetically isolated. African Journal of Ecology, 51:635 – 640.

22) Fennessy, J., Brenneman, R., 2010. Giraffa camelopardalis ssp. rothschildi. The IUCN Red List of Threatened Species. Version 2014.3. . Downloaded on 10 March 2015.

23) Fennessy, J., Brown, D., 2010. Giraffa camelopardalis. The IUCN Red List of Threatened Species. Version 2014.3. . Downloaded on 10 March 2015.

24) Frick, W. F., Pollock, J. F., Hicks, A. C., Langwig, K. E., Reynolds, D. S., Turner, G. G., Butchkoski, C. M., Kunz, T. H., 2010. An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species. Science, 329:679 – 682.

25) Giraffe Conservation Foundation, 2010. Rothschild’s giraffe joins list of species threatened by extinction. Giraffa, 4 (1):2

26) Giraffe Conservation Foundation, 2013. Africa’s Giraffe (Giraffa camelopardalis): A conservation guide. Black Eagle Media. Western Cape, South Africa.

27) Hayward, M. W., Kerley, G. I. H, 2005. Prey preferences of the lion (Panthera Leo). The Zoological Society of London, 267:309 – 322.

28) Hirst, S. M., 1969. Populations in a Transvaal Lowveld Nature Reserve, Zoologica Africana, 4 (2):199 – 230. DOI: 10.1080/00445096.1969.11447372

29) Huijibregts, B., De Wachter, P., Sosthène, L., Obiang, N., Akou, M. E., 2003. Ebola and the decline of gorilla (Gorilla gorilla) and chimpanzee (Pan troglodytes) populations in Minkebe Forest, north-eastern Gabon. Oryx, 37 (4):1 – 7.

30) Hunter, L., Wallace, D., 2001. Lumpy skin disease in southern Africa: a review of the disease and aspects of control. Journal of South African Veterinary Association, 72 (2):68 – 71.

31) Jones, M. E., Jarman, P. J., Lees, C. M., Hesterman, H., Hamede, R. K., Mooney, N. J., Mann, D., Pukk, C. E., Bergfeld J., McCallum, H., 2007. Conservation Management of Tasmanian Devils in the Context of an Emerging, Extinction-threatening Disease: Devil Facial Tumor Disease. EcoHealth, 4:326 – 337.

32) Kalema, G., 1996. Investigation of a skin disease in giraffe in Murchison Falls National Park. Report submitted to Uganda National Parks and GTZ Uganda. Unpublished.

33) Karimuribo, E. D., Mboera, L. E. G., Mbugi, E., Simba, A., Kivaria, F. M., Mmbuji, P., Rweyemamu, M. M., 2011. Are we prepared for emerging and re-emerging diseases? Experience and lessons from epidemics that occurred in Tanzania during the last five decades. Tanzania Journal of Health Research, 13:1 – 14.

34) Karstad, L. Kaminjolo, J. S., 1978. Skin Papillomas in an impala (Aepyceros melampus) and a giraffe (Giraffa camelopardalis). Journal of Wildlife Diseases, 14 (3):309 – 313.

35) Kistemann, T., Dangendorf, F., Schweikart, J., 2002. New perspectives on the use of Geographical Information Systems (GIS) in environmental health sciences. International Journal of Hygiene and Environmental Health, 205 (3):169 – 181. DOI: 10.1078/1438-4639-00145

36) Kitron, U., 1998. Landscape Ecology and Epidemiology of Vector-Borne Diseases: Tools for Spatial Analysis. Journal of Medical Entomology, 35 (4):435 – 445. DOI: 10.1093/jmedent/35.4.435

37) Kuiken, T., Wobeser, G., Leighton, F. A., Haines, D. M., Chelack, B., Bogdan, J., Hassard, L., Heckert, R. A., Riva, J., 1999. Pathology of Newcastle Disease in Double-Crested Cormorants from Saskatchewan, with comparison of Diagnostic Methods. Journal of Wildlife Diseases, 35 (1):8 – 23.

38) Lee, E. D., Bond, M. L., 2012. Giraffe Skin Disease (GSD): Epidemiology of an emerging disease. Poster presented at: AZA 2012 Annual Conference; 2012 Sep 8 – 13, Phoenix, Az, USA.

39) Leroy, E. M., Rouquet, P., Formenty, P., Souquière, S., Kilbourne, A., Froment, J., Bermejo, M., Smit, S., Karesh, W., Swanepoel, R., Zaki, S. R., Rollin, P. E., 2004. Multiple Ebola Virus Transmission Events and Rapid Decline of Central African Wildlife. Science 303:387 – 390.

40) Leuthold, B. M., 1979. Social organization and behaviour of giraffe in Tsavo East National Park. African Journal of Ecology, 17 (1):19 – 34. DOI: 10.1111/j.1365-2028.1979.tb00453.x

41) Mach, L. D., Goyal, S. M., Paul, W. J., Newton, W. E., 2008. Demographic effects of canine parvovirus on a free-ranging wolf population over 30 years. Journal of Wildlife Diseases, 44 (4):824 – 836.

42) McCallum, H., Jones, M., Hawkins, C., Hamede, R., Lachish, S., Sinn, D. L., Beeton, N., Lazenby, B., 2009. Transmission Dynamics of Tasmanian Devil Facial Tumor Disease may lead to Disease-Induced Extinction. Ecology, 90 (12):3379 – 3392.

43) McCallum, H., Tompkins, D. M., Jones, M., Lachish, S., Marvanek, S., Lazenby, B., Hocking, G., Wiersma, J., Hawkins, C. E., 2007. Distribution and Impacts of Tasmanian Devil Facial Tumor Disease. EcoHealth, 4:318 – 325.

44) Montgomery, R., Muneza, A., 2015. Scratching at the surface of Giraffe Skin Disease. Giraffid, 9 (1):15.

45) Mpanduji, D. G., Karimuribo, E., Epaphras, A. M., 2011. Investigation of Giraffe Skin Disease of Ruaha National Park, Southern Highlands of Tanzania. Tanzania National Parks. Unpublished.

46) Mutinda, M., Otiende, M., Gaya, F., Kariuki, L., Obanda, V., Ndeere, D., Ndambiri, E., Kariuki, E., Lekolool, I., Soriguer, R. C., Rossi, L., Alasaad, S., 2012. Putative filariosis outbreak in white and black rhinoceros at Meru National Park in Kenya. Parasites and Vectors, 5:206 – 210.

47) Normile, D. 2008. Driven to Extinction. Science, 5870 (319): 1606 – 1609.

48) Pelkey, N. W., Stoner, C. J., Caro, T. M., 2000. Vegetation in Tanzania: assessing long term trends and effects of protection using satellite imagery. Biological Conservation, 94 (2000):297 – 309.

49) Randall, D. A., Marino, J., Haydon, D. T., Sillero-Zuburi, C., Knobel, D. L., Tallents, L. A., Macdonald, D. W., Laurenson, M. K., 2006. An integrated disease management strategy for the control of rabies in Ethiopian wolves. Biological Conservation, 131(2):151 – 162. DOI: 10.1016/j.biocon.2006.04.004

50) Seeber, A. P, Ciofolo, I., Ganswindt, A., 2012. Behavioral inventory of the giraffe (Giraffa camelopardalis). BioMed Central Research Notes 5:650 – 657.

51) van der Jeugd, H. P., Prins, H. H. T., 2000. Movements and group structure of giraffe (Giraffa camelopardalis) in Lake Manyara National Park, Tanzania. Journal of Zoology, 251 (1):15 – 21. DOI: 10.1111/j.1469-7998.2000.tb00588.x

52) van Dyk, E., Bosman, A. M., van Wilpe, E., Williams, J. H., Bengis, R. G., van Heerden, J., Venter, E. H., 2011. Detection and characterization of papillomavirus in skin lesions of giraffe and sable antelope in South Africa. Journal of the South African Veterinary Association, 82(2):80 – 85.

53) Voyles, J., Young, S., Berger, L., Campbell, C., Voyles, W. F., Dinudom, A., Cook, D., Webb, R., Alford, R. A., Skerratt, L. F., Speare, R., 2009. Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science, 326:582 – 585.

54) Woods, J. A., 1988. Lumpy Skin Disease: A review. Tropic Animals Health and Production 20:11 – 17.

55) World Conservation Society, 2013. Preliminary Report on Ruaha Giraffe Skin Disease. Report submitted to TANAPA Veterinary Unit. Unpublished.

56) Young, E. E., 1970. Experimental infection of game animals with lumpy skin disease virus (prototype strain Neethling). Onderstepoort Journal of Veterinary Research, 37 (2):79 – 87.

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.

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 non- invasive 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 spatially- explicit 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 km2) 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 road- less and mostly inaccessible to vehicles.

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 (푥̅ = 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 geo- referenced. 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:

22 λij λ0 ij  exp d ij 2σ i 

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 ψGSD 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

2 per km (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.

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.

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.

APPENDIX

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

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]

α1 male –0.45 [–0.83, –0.08]

α2 subadult 0.48 [–0.15, 1.10]

α3 male × subadult –0.62 [–1.53, 0.29]

α4 # severe legs –0.04 [–0.19, 0.24]

δ0 0.91 [0.79, 1.02]

δ1 male 0.13 [–0.02, 0.32]

δ2 subadult –0.36 [–0.56, –0.01]

δ3 male × subadult 0.61 [0.14, 0.96]

δ4 # severe legs –0.07 [–0.16, 0.03] N 1819 [1614, 2040] D 0.55 [0.49, 0.62]

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.

REFERENCES

1) Abade, L., Macdonald, D. W. and A. J. Dickman. 2014. Using landscape and bioclimatic features to predict the distribution of lions, leopards and spotted hyaenas in Tanzania’s Ruaha landscape. PLoS ONE 9(5):e96261

2) Alasaad, S., Ndeereh, D., Rossi, L., Bornstein, S., Permunian, R., Soriguer, R. C. and F. Gakuya. 2012. The opportunistic Sarcoptes scabiei: A new episode from giraffe in the drought-suffering Kenya. Veterinary Parasitology 185:359 – 363

3) Bendik, N. F., Morrison, T. A., Gluesenkamp, A. G., Sanders, M. S. and L. J. O’Donell. 2013. Computer-Assisted Photo Identification Outperforms Visible Implant Elastomers in an Endangered Salamander, Eurycea tonkawae. PLoS ONE, 8 (3):e59424

4) Bercovitch F. B. and P. S. M. Berry. 2013. Herd Composition, Kinship and Fission-Fusion Social Dynamics among Wild Giraffe. African Journal of Ecology, 51:206 – 216

5) Bolger, D. T., T. A. Morrison, B. Vance, D. Lee and H. Farid. 2012. A computer-assisted system for photographic mark-recapture analysis. Methods in Ecology and Evolution 3:813 – 822

6) Borchers, D.L. and Efford, M.G. 2008. Spatially explicit maximum likelihood methods for capture-recapture studies. Biometrics, 64, 377-385.

7) Brown, M. B. and J. Fennessy. 2014. A preliminary assessment of Rothschild’s giraffe in Uganda. Giraffe Conservation Foundation.

8) Cecchi, G., Mattioli, R. C., Slingenbergh, J. and S. De La Rocque. 2008. Land cover and tsetse fly distributions in sub-Saharan Africa. Medical and Veterinary Entomology, 22:364 – 373.

9) Daszak, P., Cunningham, A. A. and A. D. Hyatt. 2000. Emerging Infectious Diseases of Wildlife-Threats to Biodiversity and Human Health. Wildlife Ecology, 287:443 – 448

10) 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

11) Epaphras, A. M., Gereta, E., Lejora, I. A., Ole Meing’ataki, G. E., Ng’umbi, G., Kiwango, Y., Mwangomo, E., Semanini, F., Vitalis, L., Balozi, J., and M. G. G. Mtahiko. 2007. Wildlife water utilization and importance of artificial waterholes during dry season at Ruaha National Park, Tanzania. Wetlands Ecology and Management, 16 (3):183 – 188.

12) Fennessy, J. T. 2009. Home Range and Seasonal Movements of Giraffa Camelopardalis angolensis in the northern Namib Desert. African Journal of Ecology, 47(3):318 – 327

13) Ferreira, S. M. and P. J. Funston. 2010. Estimating lion population variables: prey and disease effects in Kruger National Park, South Africa. Wildlife Research 37:194 – 206

14) Foster, R. J., and B. J. Harmsen. 2012. A critique of density estimation from camera-trap data. Journal of Wildlife Management 76:224-236.

15) Gelman, A., Carlin, J.B., Stern, H.S., Dunson, D.B., Vehtari, A. and D. B. Rubin. 2013 Bayesian data analysis, 3rd edn. CRC Press, Boca Raton, FL.

16) Gerber, B., S. M. Karpanty, C. Crawford, M. Kotschwar and J. Randrianantenaina. 2010. An assessment of carnivore relative abundance and density in the eastern rainforests of Madagascar using remotely-triggered camera traps. Oryx 44 (2):219 – 222

17) Giraffe Conservation Foundation. 2010. Rothschild’s giraffe joins list of species threatened by extinction. Giraffa 4(1):2

18) Giraffe Conservation Foundation. 2013. Africa’s Giraffe (Giraffa camelopardalis): A conservation guide. Black Eagle Media. Western Cape, South Africa

19) Gompper, M. E., R. W. Kays, J. C. Ray, S. D. Lapoint, D. A. Bogan, and J. R. Cryan. 2006. A comparison of Noninvasive Techniques to Survey Carnivore Communities in Northeastern North America. Wildlife Society Bulletin 34(4):1142 – 1151

20) Gortázar, C., Acevedo, P., Ruiz-Fons, F. and J. Vicente. 2006. Disease Risks and Overabundance of Game Species. European Journal of Wildlife Research, 52 (2):81 – 87

21) Hammond, E. E., Miller, C. A., Sneed, L. and R. W. Radcliffe. 2003. Mycoplasma-associated Polyarthritis in a Reticulated Giraffe. Journal of Wildlife Diseases 39 (1):233 – 237

22) Hirst, S. M. 1969. Populations in a Transvaal Lowveld Nature Reserve. Zoologica Africana, 4(2):199 – 230

23) Hunter, L. and D. Wallace. 2001. Lumpy skin disease in southern Africa: a review of the disease and aspects of control. Journal of South African Veterinary Association, 72 (2):68 – 71.

24) International Giraffe Working Group. 2012. Extant giraffe taxonomy: statement from the IUCN SSC ASG International Giraffe Working Group. Giraffa 6(1):2

25) International Union of Conservation Nature. 2007. Regional Conservation Strategy for the Cheetah and African Wild Dog in Eastern Africa. Gland, Switzerland.

26) Kaitho, T., Ndeereh, D. and B. Ngoru. 2013. An Outbreak of anthrax in endangered Rothschild’s giraffes in Mwea National Reserve, Kenya. Veterinary Medicine: Research and Reports 4:45 – 48

27) Kalema, G. 1996. Investigation of a skin disease in giraffe in Murchison Falls National Park. Uganda National Parks. Kampala, Uganda.

28) Karanth, K. U., J. D. Nichols, N. S. Kumar and J. E. Hines. 2006. Assessing Tiger Population Dynamics Using Photographic Capture – Recapture Sampling. Ecology 87 (11):2925 – 2937

29) Karimuribo, E. D., L. E. G. Mboera, E. Mbugi, A. Simba, F. M. Kivaria, P. Mmbuji and M. M. Rweyemamu. 2011. Are we prepared for emerging and re-emerging diseases? Experience and lessons from epidemics that occurred in Tanzania during the last five decades. Tanzania Journal of Health Research 13:1 – 14

30) Karstad, L. and J. S. Kaminjolo. 1978. Skin Papillomas in an impala (Aepyceros melampus) and a giraffe (Giraffa camelopardalis). Journal of Wildlife Diseases, 14 (3):309 – 313

31) Keawcharoen, J., K. Oraveerakul., T. Kuiken, R. A. M. Fouchier, A. Amonsin, S. Payungporn, S. Noppornpath, S. Wattanodorn, A. Theamboonlers, R. Tantilertcharoen, R. Pattanarangsan, N. Arya, P. Ratanakorn, A. D. M. E. Osterhaus and Y. Poovorawan. 2004. Avian Influenza H5N1 in Tigers and Leopards. Emerging Infectious Diseases 10 (12):2189 – 2191

32) Kellner, K. 2014. jagsUI: Run JAGS (specifically, libjags) from R; an alternative user interface for rjags. R package version 1.1.

33) Kéry, M., Gardner, B., Stoeckle, T., Weber, D. and J. A. Royle. 2011. Use of Spatial Capture- Recapture Modeling and DNA Data to Estimate Densities of Elusive Animals. Conservation Biology 25 (2):356 – 364

34) Kolmstetter, C., L. Munson and E. C. Ramsay. 2000. Degenerative Spinal Disease in Large Felids. Journal of Zoo and Wildlife Medicine 31(1):15 – 19

35) Langwig, K. E., Frick, W. F., Bried, J. T., Hicks, A. C., Kunz, T. H. and A. M. Kilpatrick. 2012. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters 15:1050 – 1057

36) Lee, D. E. 2015. Demography of Giraffe in the fragmented Tarangire Ecosystem. PhD Dissertation. Dartmouth College.

37) Lee, D. E. and M. L. Bond. 2013. Giraffe Skin Disease (GSD): Epidemiology of an emerging disease. Unpublished data.

38) Liccioli, S., Rogers, S., Greco, C., Kutz, S. J., Chan, F., Ruckstuhl, K. E. and A. Massolo. 2015. Assessing individual patterns of Echinococcus multilocularis infection in urban coyotes: non- invasive genetic sampling as an epidemiological tool. Journal of Applied Ecology 52:434 – 442

39) Lowe, D. G. 2004. Distinctive Image Features from Scale-Invariant Keypoints. International Journal of Computer Vision 60 (2), 91-110

40) Lunn, D. J., Thomas, A., Best, N. and D. Spiegelhalter. 2000. WinBUGS - A Bayesian modelling framework: Concepts, structure, and extensibility. Statistics and Computing, 10, 325- 337.

41) Marucco, F., D. H. Pletcher, L. Boitani, M. K. Schwartz, K. L. Pilgrim and J. Lebreton. 2009. Wolf survival and population trend using non-invasive capture – recapture techniques in the Western Alps. Journal of Applied Ecology 46:1003 – 1010

42) National Bureau of Statistics. 2013. Tanzania in figures 2012. Ministry of Finance and Economic Affairs. Dar es Salaam, Tanzania

43) Piotrowski, J. S., Annis, S. L. and J. E. Longore. 2004. Physiology of Batrachochytrium dendrobatidis, a Chytrid Pathogen of Amphibians. Mycologia, 96 (1):9 – 15

44) Plummer, M. 2003. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd international workshop on distributed statistical computing. Vienna, Austria.

45) R Core Team. 2015. R: A language environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

46) Riggio, J., A. Jacobson, L. Dollar, H. Bauer, M. Becker, A. Dickman, P. Funston, R. Groom, P. Henschel, H. de Iongh, L. Lichtenfeld and S. Pimm. 2012. The size of savannah Africa: a lion’s (Panthera leo) view. Biodiversity and Conservation 22:17 – 35

47) Royle, J. A. and K. V. Young. 2008. A hierarchical model for spatial capture-recapture data. Ecology, 89, 2281-2289.

48) Royle, J. A., A. J. Magoun, B. Gardner, P. Valkenburg, and R. E. Lowell. 2011. Density estimation in a wolverine population using spatial capture-recapture models. Journal of Wildlife Management 75:604-611.

49) Royle, J. A. and R. Dorazio. 2012. Parameter-expanded data augmentation for Bayesian analysis of capture–recapture models. Journal of Ornithology, 152, S521-S527.

50) Royle, J. A., Chandler, R. B., Sollmann, R. and B. Gardner. 2014. Spatial capture-recapture. Academic Press, Waltham, MA, USA.

51) Seimon, T. A., D. G. Miquelle, T. Y. Chang, A. L. Newton, I. Korotkova, G. Ivanchuk, E. Lyubchenko, A. Tupikov, E. Slabe and D. McAloose. 2013. Canine distemper virus: an emerging disease in wild endangered Amur Tigers (Panthera tigris altaica). mBio 4(4):e00410 – e00413

52) Soisalo, M. K., and S. M. C. Cavalcanti. 2006. Estimating the density of a jaguar population in the Brazilian Pantanal using camera-traps and capture-recapture sampling in combination with GPS radio-telemetry. Biological Conservation 129:487-496.

53) Sollmann, R., M. M. Furtado, B. Gardner, H. Hofer, A. T. A. Jàcomo, N. M. Tôrres and L. Silveira. 2011. Improving density estimates for elusive carnivores: Accounting for sex-specific detection and movements using spatial capture-recapture models for jaguars in central Brazil. Biological Conservation 144:1017 – 1024

54) Stoner, C., Caro, T., Mduma, S., Mlingwa, C., Sabuni, G. and M. Borner. 2007. Assessment of Effectiveness of Protection Strategies in Tanzania Based on a Decade of Survey Data for Large Herbivores. Conservation Biology, 21(3):635 – 646

55) Strauss, M. K. L. 2014. Ecological and Anthropogenic Drivers of giraffe (Giraffa camelopardalis tippelskirchi) population dynamics in the Serengeti. PhD Dissertation. University of Minnesota.

56) Thorn, M., M. Green, P. W. Bateman, S. Waite and D. M. Scott. 2011. Brown hyaenas on roads: Estimating carnivore occupancy and abundance using spatially auto-correlated sign survey replicates. Biological Conservation 144:1799 – 1807

57) van Dyk, E., Bosman, A. M., van Wilpe, E., Williams, J. H., Bengis, R. G., van Heerden, J. and E. H. Venter. 2011. Detection and characterization of papillomavirus in skin lesions of giraffe and sable antelope in South Africa. Journal of the South African Veterinary Association, 82 (2):80 – 85

58) Wake, D. B. 2007. Climate Change Implicated in Amphibian and Lizard Declines. Proceedings of the National Academy of Sciences of the United States of America, 104 (20):8201 – 8202

59) Young, A. and S. L. Monfort. 2009. Stress and the costs of extra-territorial movement in a social carnivore. Biology Letters 5:439 – 441

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 sub-

Saharan 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 capture- recapture 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 individually- recognizable 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

73 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.

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.