Pangolins in Peril: a Perspective of Their Use As Traditional

PANGOLINS IN PERIL: A PERSPECTIVE OF THEIR USE AS TRADITIONAL

MEDICINE AND BUSHMEAT IN WEST AFRICA

Maxwell Kwame Boakye

Submitted in partial fulfilment of the requirements for the degree

DOCTOR TECHNOLOGIAE

in the

Department of Environmental, Water and Earth Sciences

FACULTY OF SCIENCE

TSHWANE UNIVERSITY OF TECHNOLOGY

Supervisor: Prof Raymond Jansen

Co-supervisor: Prof Antoinette Kotzé

Co-supervisor: Dr Desiré-Lee Dalton

September 2016 DECLARATION BY CANDIDATE

“I hereby declare that the thesis submitted for the degree D. Tech: Environmental

Management, at Tshwane University of Technology, is my original work and has not previously been submitted to any other institution of higher education. I further declare that all sources cited or quoted are indicated and acknowledged by means of a compressive list of references”.

Maxwell Kwame Boakye

DEDICATION

This study is dedicated to the following family members for their encouragement and support in all my endeavours: Anna Gyamfi, Dorothy Serwaa Boakye, Dennis Appiah Boakye,

Dominic Opoku Boakye, Linda Adwubi Amankwaa, Gabriela Owusuwaa Nkunim Otoo

Sakum and Abena Gyamfua Boakye.

ACKNOWLEDGMENTS

First and foremost, I would like to thank my supervisors, Prof Raymond Jansen, Prof

Antoinette Kotzé and Dr Desiré-Lee Dalton for their encouragement, advice, constructive criticism and general assistance. I am very grateful to Prof Raymond Jansen, for admitting me and agreeing to supervise this research. I am also grateful to Darren Pietersen of the African

Pangolin Working Group for his assistance in conceptualizing this research.

My gratitude also goes to all the traditional chiefs and opinion leaders who agreed to allow this research to be undertaken in their communities for their assistance and support. To the traditional healers, farmer hunters, bushmeat wholesalers and chopbar operators who took part in this research, I would like to say thank you for making this study a success. From the field, firstly I would like to thank Nana Kwadwo Pipim, Nuru Gadafi and Ibrahim Iddirisu,

Pastor Kelfala Kanu and Mahmoud Bayon for their assistance during field data collection.

I am also thankful to Dr Benjamin Akpor, Dr Alfred Kanu, Dr Peter Dosu, Dr Kefani

Kedabe, and Mr Yaw Baffoe for their friendly support and encouragement during my study.

I express my deep appreciation and thanks to my Dad (Mr Johnson Boakye-Apomasuh), and

Mom (Mrs Lydia Appiah Boakye), uncle (Dr A. A. Asare-Bediako) and cousin (Mr Frederick

Asare-Bediako) for their support and encouragement.

For financial support, I would like to acknowledge and thank the Rufford Small Grant

Foundation (Grant Number 13600-1), the National Zoological Gardens of South Africa and the Tshwane University of Technology for their support.

iii

ABSTRACT

Pangolins (Pholidota: Manidae) form an important part of local cultures and traditions in the majority of central and west African countries. The use of whole pangolins or body parts for medicinal purposes in Africa is long-established and they are also hunted as a source of bushmeat across the continent. However, very little is known about the cultural importance of pangolin body parts that are used to treat, alleviate or cure particular ailments and diseases as well as the level of trade for bushmeat purposes in west Africa. In addition, the level of local knowledge relating to pangolins and how it can be integrated with scientific ecological knowledge to contribute to implementation plans and conservation management actions for pangolins in the forests of west Africa has not been determined. The aim of this study was to determine the traditional medicinal importance of pangolins to local communities, pangolin level of trade for bushmeat purposes and local ecological knowledge amongst collectors of pangolins.

Using purposive and snowball sampling for the selection of participants, data were gathered on traditional medicinal use, level of trade for bushmeat purposes as well as level of local ecological knowledge of hunters using semi-structured interviews. Ethnozoological data on the use of pangolins for traditional medicinal purposes were collected from 63 and 48 traditional healers in Sierra Leone and Ghana, respectively. Data were gathered from 153 stakeholders comprising chopbar operators, farmer hunters and wholesalers to determine the level of trade in Ghana. Information on the level of local ecological knowledge of hunters was gathered from 126 and 153 farmer hunters in Sierra Leone and Ghana, respectively.

Ethnozoological data were analysed using use value, cultural importance and informant agreement ratio indices. A total of 21 pangolin parts and tissue oil was found to be used to treat various ailments in Sierra Leone while 13 body parts were used to treat various ailments

iv in Ghana. Pangolin scales were the most culturally important body part according to the rank at which this body part was used in both countries. The results revealed that pangolin body parts play a vital role in the primary healthcare of the people in both countries. A total of 341 pangolins were recorded to have been traded during the study period and, of this number, 98 pangolins were personally observed. Three species of African pangolin are known to occur in both countries. Of these 82% of pangolins traded were white-bellied pangolin (Phataginus tricuspis) while 18% where black-bellied pangolin (Phataginus tetradactyla), with no trade observed for the giant ground pangolin (Smutsia gigantea). Local ecological knowledge of farmer hunters revealed that they were familiar with two of the three African pangolin species that occur in Ghana and Sierra Leone, i.e. the arboreal black-bellied pangolin (P. tetradactyla) and white-bellied pangolin (P. tricuspis) but none reported hunting the giant ground pangolin (S. gigantea).

Although in existence, current legislation has been unable to combat harvesting of pangolins for traditional therapeutic and dietary purposes. The Wildlife Conservation Act in both Ghana and Sierra Leone prohibits any person from hunting or being in possession of pangolins, however, enforcement is lacking. In addition, pangolins are listed in the Convention on

International Trade in Endangered Species (CITES) as Appendix II and were up-listed as vulnerable on the recently revised International Union for Conservation of Nature Red List. It is highly likely that the unregulated harvesting and poaching of this threatened group of mammals for medicinal purposes and the bushmeat market, is completely unsustainable. A study to determine the population status and ecology of the three species of African pangolins occurring in both countries is urgently required in order to assess the impact of harvesting on the populations which is currently unmonitored and unsustainable. Within this context, there is an urgent need to determine pangolin population abundance within the region, and Africa in general, to ensure their survival.

CONTENTS

PAGE

DECLARATION i

DEDICATION ii

ACKNOWLEDGEMENTS iii

ABSTRACT iv

LIST OF FIGURES xi

LIST OF TABLES xiii

LIST OF PLATES xv

CHAPTER 1

1 INTRODUCTION 1

1.1 Background and Motivation 1

1.2 Motivation for study 2

1.3 Research objectives 4

1.4 Study localities 4

1.5 Motivation for choice of study countries 7

1.6 Thesis structure 9

CHAPTER 2

2 GENERAL LITERATURE REVIEW 10

2.1 General morphological characteristics of pangolins 10

2. 2 Taxonomy and general characteristics of African pangolins 11

2.2.1 White-bellied pangolin (P. tricuspis) 14

2.2.2 Black-bellied pangolin (P. tetradactyla) 15

2.2.3 Giant ground pangolin (S. gigantea) 16

2.2.4 Temminck’s ground pangolin (S. temminckii) 17

2.3 Habitat and distribution 18

2.4 Conservation status and threats 21

CHAPTER 3

3 ETHNOMEDICINAL USE OF AFRICAN PANGOLINS BY TRADITIONAL

MEDICAL PRACTITIONERS IN SIERRA LEONE 24

3.1 Introduction 24

3.2 Materials and methods ` 26

3.2.1 Study site 26

3.2.2 Ethics Statement 27

3.2.3 Data collection 28

3.3 Data analysis 29

3.3.1 Use Value (UV) 29

3.3.2 Informant Agreement Ratio (IAR) 30

3.3.3 Use Agreement Value (UAV) 31

3.4 Results 31

3.5 Discussion 41

3.5.1 Use value (UV) 41

3.5.2 Informant Agreement Ratio (IAR) 43

3.5.3 Comparing different indices 44

3.6 Conservation implications 45

3.7 Conclusion 48

vii

CHAPTER 4

4 KNOWLEDGE AND USES OF AFRICAN PANGOLINS AS A SOURCE OF

TRADITIONAL MEDICINE IN GHANA 50

4.1 Introduction 50

4.2 Materials and Methods 52

4.2.1 Study area 52

4.2.2 Ethics Statement 53

4.2.3 Data collection 53

4.3 Data analysis 54

4.3.1 Cultural Importance Index (CI) 54

4.3.2 Relative Frequency of Citation (RFC) 55

4.3.3 Informant Agreement Ratio (IAR) 55

4.3.4 Use Agreement Value (UAV) 56

4.4 Results 56

4.5 Discussion 65

4.5.1 Cultural importance index (CI) 65

4.5.2 Informant Agreement Ratio (IAR) 66

4.5.3 Comparing different indices 68

4.6 Conservation implications 69

4.7 Conclusion 71

CHAPTER 5

5 UNRAVELLING THE PANGOLIN BUSHMEAT COMMODITY CHAIN AND

THE EXTENT OF TRADE IN GHANA 73

5.1 Introduction 73

viii

5.2 Materials and methods 75

5.2.1 Study area 75

5.2.2 Ethics statement 76

5.2.3 Data collection 76

5.2.4 Statistical analyses 78

5.3 Results 79

5.4 Discussion 84

5.5 Conservation implications 87

5.6 Conclusion 88

CHAPTER 6

6 LOCAL ECOLOGICAL KNOWLEDGE OF PANGOLINS AMONG HUNTERS IN

GHANA AND SIERRA LEONE 90

6.1 Introduction 90

6.2 Materials and methods 92

6.2.1 Study area 92

6.2.2 Ethics statement 93

6.2.3 Data collection 94

6.3 Data analysis 95

6.4 Results 95

6.4.1 General morphological characteristics 97

6.4.2 General ecology and diet 97

6.4.3 Temporal relative patterns of abundance 98

6.4.4 Reproductive biology 99

6.4.5 Cultural and conservation issues 100

6.5 Discussion 101

6.6 Conservation implications 105

6.7 Conclusion 106

CHAPTER 7

7 SYNTHESIS 108

REFERENCES 112

APPENDIX 1

QUESTIONNAIRE 150

LIST OF FIGURES

FIGURE 1.1: Map of Africa indicating locations of Ghana and Sierra Leone 5

FIGURE 2.1: Phylogeny of Pholidota based on PAUP

(Phylogenetic Analysis Using Parsimony) analysis of 395 osteological

characters in 15 ingroup taxa, including seven of the eight extant pangolin

species, five fossil pangolins, Eurotamandua joresi, and two

metacheiromyid palaeanodont genera, Palaeanodon and Metacheiromys

(Adapted from Gaudin, Emry & Wible, 2009) 13

FIGURE 2.2: Distribution of the four African pangolin species (Adapted from

Challender, Waterman & Baillie, 2014) 19

FIGURE 3.1: Map of Africa indicating Sierra Leone and the study

district of Bombali 27

FIGURE 5.1: Map of Africa indicating Ghana’s administrative regions

and the study sites 75

FIGURE 5.2: Trade flow patterns in the pangolin bushmeat commodity chain 80

FIGURE 5.3: Total number of pangolins traded for all study sites by all stakeholders in

each study month 81

FIGURE 5.4: Mean number of pangolins traded by stakeholder groups in each study

month 82

FIGURE 5.5: The negative relationship between the distance from where pangolins are

sourced in protected areas and the number traded in all sites by all

stakeholders 83

FIGURE 6.1: Map of the study regions in Ghana and Sierra Leone 93

FIGURE 6.2: Age group and regional response to alternative diet for

pangolins in Ghana 98

FIGURE 6.3: Birth frequency and litter size response among palm wine tappers

(PWT), farmer hunters in Sierra Leone (FHSL) and farmer hunter

in Ghana (FHGH) 100

xii

LIST OF TABLES

TABLE 3.1: Use of pangolin body parts and the prescribed conditions treated, Use

Report (UR) and International Classification of

Diseases (ICD) categories 34

TABLE 3.2: Use Value (UV) of pangolin body parts for each International Classification

of Diseases (ICD) category 36

TABLE 3.3: Informant Agreement Ratio (IAR) of pangolin body parts for each

International Classification of Diseases (ICD) category 38

TABLE 3.4: Evaluation of pangolin body parts using Use Value (UV), Informant

Agreement Ratio (IAR) and Use Agreement Value (UAV) 40

TABLE 4.1: Demographics of participants in the study 57

TABLE 4.2: Use Report (UR) by traditional healers for particular pangolin body parts

for the treatment of specific ailments 58

TABLE 4.3: Cultural Importance Index (CI) of pangolin body parts and their respective

ailments treated 60

TABLE 4.4: Informant Agreement Ratio (IAR) of pangolin body parts and their

respective ailments treated 62

xiii

TABLE 4.5: Evaluation of pangolin body parts using Cultural Importance Index (CI),

Relative Frequency of Citation (RFC), Informant Agreement Ratio (IAR)

and Use Agreement Value (UAV) 64

TABLE 5.1: Number of pangolin species physically observed to be traded by

stakeholders 79

TABLE 6.1: Demographics of the people interviewed in both Ghana and

Sierra Leone 96

xiv

LIST OF PLATES

PLATE 2.1: White-bellied pangolin 14

PLATE 2.2: Black-bellied pangolin 15

PLATE 2.3: Giant ground pangolin 17

PLATE 2.4: Temminck’s ground pangolin 18

CHAPTER 1

INTRODUCTION

1.1 Background and Motivation

Humans and animals coexist in an elaborate relationship in all societies (Bagniewska &

Macdonald, 2010; Alves, 2012). Amongst the most fundamental uses of animals by humans are to meet their nutritional needs and derive products in the preparation of curative, protective and preventive medicine mostly in the form of traditional medicine (Adeola, 1992;

Alves, 2012). Furthermore, it is estimated that half of the world’s population rely on traditional medicine to meet their daily healthcare needs (WHO, 2000; WHO, 2002; WHO,

2010a) and incorporate animal-derived products obtained from wild and domestic animals and their by-products in the preparation of therapeutics remedies (Adeola, 1992; Alves &

Alves, 2011; Alves & Rosa, 2012; Ashwell & Walston, 2008; Whiting, Williams & Hibbitts,

2011). In general, wildlife are also often used as a key source of animal protein in tropical regions but dependence on wild meat is most abundant in many west and central African countries (Anadu, Elamah & Oates, 1988; Bowen-Jones, Brown & Robinson, 2002; Fa et al.,

2002; Brashares et al., 2004; Parliamentary Office Of Science And Technology (POST),

2005; Albrechtsen et al., 2007; Waite, 2007; Nasi et al., 2008; Fa & Brown, 2009; Allebone-

Webb et al., 2011; Golden et al., 2011; Schulte-Herbrüggen et al., 2013a, b).

The use of animals for traditional medicine and food is a major cause of overexploitation of numerous species and appears to have a significant detrimental impact on wild populations

(Bennett & Rao, 2002; Still, 2003; Alves & Rosa, 2005; Costa-Neto, 2005; Alves, 2012).

This utilization has further been described as one of the greatest threats contributing to the decline of certain species of wild animals (Adeola, 1992; Redford, 1992; Wilkie et al., 1998,

Peres, 2000; Fa et al., 2002; Still, 2003, Costa-Neto, 2005; Soewu, 2008; Alves, 2012;

Djagoun et al., 2013; Soewu, 2013). The majority of the species utilized today for traditional medicinal and bushmeat purposes are listed as threatened or endangered with both practices contributing to serious population declines and possibly contributing directly to species extinctions (Anyinam, 1995; Oates et al., 2000; Brashares, Arcese & Sam, 2001; Brashares et al., 2004; Albrechtsen et al., 2007; Fa & Brown, 2009; Alves, 2012; Djagoun et al., 2013;

Soewu, 2013). Pangolins are a group of mammals that have been hunted for their purported traditional medicinal values and as a source of bushmeat in Africa through known history and this practice continues till date (Sodeinde & Adedipe, 1994; Gaubert, 2011; Soewu &

Sodeinde, 2015).

1.2 Motivation for study

In ethnobiological studies, it is no longer sufficient to merely and uncritically provide lists of species or body parts used without information about the cultural importance of these species or body parts (Heinrich et al., 2009). A review of the literature indicates that traditional medicinal use of pangolins in Africa has focused on uncritical listing of whole or body parts of pangolins and ailments treated and little attention has been placed on the cultural importance or otherwise of pangolins and their body parts utilized within local African communities. Consequently, relatively little is known about the use value and cultural importance of pangolins to traditional medical practitioners and local communities as a whole. Also, most of the literature on pangolin bushmeat trade focused on surveys of major commercial bushmeat markets to determine trends in pangolin bushmeat trade and

2 consumption. However, evidence suggest that not all bushmeat reach the major bushmeat markets due to a multiplicity of factors including distance to major bushmeat markets, size of the animal as well as sales at village level (Fa et al., 1995; Fa et al., 2006; Crookes et al.,

2007; Allebone-Webb et al., 2011; Kamins et al., 2011; Weinbaum et al., 2013). As such, market surveys have therefore been relatively inadequate in quantifying wildlife utilisation in

Africa (Hofmann, Ellenberg & Roth, 1999). As a result, this hampers our ability to estimate the level of pangolin utilization and harvest from natural wild populations and the movement along the informal bushmeat commodity chain. The bushmeat commodity chain has been partly characterised in Africa (Mendelson, Cowlishaw & Rowcliffe, 2003; Cowlishaw,

Mendelson & Rowcliffe, 2004; Cowlishaw, Mendelson & Rowcliffe, 2005a, b), yet studies that assess pangolin bushmeat trade have not been undertaken to determine the extent and level of trade locally within African countries.

Most importantly, there is little scientific information about the biology and ecology of the four African pangolin species (Gaudin, Emry & Wible, 2009; Gaubert, 2011; Kingdon &

Hoffman, 2013; Challender, Waterman & Baillie, 2014; Challender et al., 2014). Although local ecological knowledge (LEK) has been proven to be useful in expanding the sources of information for ecosystem management and yielded benefits to conservation outcomes

(Berkes, 1993; Olsson & Folke, 2001; Huntington, 2000; Huntington et al., 2004; Baird &

Flaherty, 2005; Gilchrist, Mallory & Merkel, 2005, Sheil et al., 2006), there are no empirical studies that have explored and documented the role of LEK among hunters/collectors, especially in terms of its relative contribution to conservation planning for Africa pangolin species. By investigating the use and trade within local rural communities, this research aims to contribute towards developing a more comprehensive understanding of pangolin utilization

3 in west Africa to support a sustainable future and impact on conservation actions for pangolins in Africa.

1.3 Research objectives

The primary aim of this thesis is to explore the cultural importance of pangolins as used as a traditional medicinal animal species, their level of trade as a source of bushmeat and investigate the local ecological knowledge (LEK) of hunters/collectors.

The primary research objectives are as follows:

 to determine the use value of pangolin body parts to traditional medicinal practitioners

in Sierra Leone

 to determine the cultural value of pangolin body parts to traditional healers in Ghana

 to determine the level of pangolin bushmeat trade along the bushmeat commodity

chain in Ghana

 to determine the level of local ecological knowledge (LEK) with regards pangolins

among hunters/collectors in Ghana and Sierra Leone

1.4 Study localities

Ghana and Sierra Leone are both located on the west coast of Africa (Figure 1.1) and are situated in the Upper Guinean Rainforest that has been recognized as one of the hotspots for biodiversity conservation with large numbers of endemic species of importance to conservation (Myers et al., 2000, Kouame et al., 2012). Ghana is situated between latitudes

4°35'N and 1I°N and longitudes 3°5'W and 1°10'E with a total land area of 238,533 km2 and

4 is bordered by Togo to the east, La Cote d'Ivoire to the west, Burkina Faso to the north and the Atlantic Ocean to the south (Tamakloe, 2000; Karen & Quaye, 2006).

Figure 1.1: Map of Africa indicating locations of Ghana and Sierra Leone

The total human population of Ghana is estimated at 27,043,093 (Ghana Statistical Service,

2014). The mean annual rainfall varies between the north and the south of the country with the southwestern, southeastern and the northern portions receiving a mean maximum of 2000 mm, 1500 mm, and 1000 mm, respectively per annum (Tamakloe, 2000; Karen & Quaye,

2006; Stanturf et al., 2011). The mean monthly temperature is around 25oC but ranges from mean minimum of 21°C and mean maximum of 35°C (Tamakloe, 2000; Karen & Quaye,

2006). Based primarily on annual total rainfall and major natural vegetation types, six major ecological zones are recognised in Ghana: the Coastal Savanna Zone, Wet and Moist

Evergreen Forest Zone, Deciduous Forest Zone, Transitional Zone, Guinea Savanna Zone, and the Sudan Savanna Zone (Hall & Swaine, 1976; Tamakloe, 2000; Karen & Quaye, 2006;

Stanturf et al., 2011). The faunal diversity of the forested areas is very high accounting for about 83% of the total number of species recorded (Ministry of Environment and Science-

Ghana, 2002) where 225 mammalian species (with 93 recorded to inhabit the savanna ecological zones) have been reported with the majority of them classified as endangered or vulnerable (Ministry of Environment and Science-Ghana, 2002).

The Republic of Sierra Leone is also situated on the West Coast of Africa and is situated between latitude 6o 00' and 10o 0' N and longitude 10o 16’ W and 13o 18′ W with a total land area of approximately 72, 000 km2 and is bordered on the West by the Atlantic Ocean, by

Guinea in the North and Northeast and by Liberia on the South-East (Figure 1.1) (Blinker,

2006; Brown & Crawford, 2012; Environmental Protection Agency, 2014). Sierra Leone has a total human population of 5.9 million (United Nations Population Fund (UNFPA), 2014).

The climate is tropical with two distinct seasons, namely the wet season starting from May-

October and the dry season from November to April, each lasting for about six months with an annual rainfall ranging between 2500 mm in the drier areas and 5000 mm in the Freetown

Peninsula (Blinker, 2006). Temperatures vary from 25oC to 34oC but can drop during harmattan to 16oC.

Sierra Leone is situated at the western most extent of the Upper Guinean Rainforest and has been recognized as one of the hotspots for biodiversity conservation with a large number of endemic species (Blinker, 2006; Brown & Crawford, 2012; Environmental Protection

Agency, 2014). One hundred and seventy eight species of mammals have been identified in

Sierra Leone with most of them being classified as Endangered or Threatened

(Environmental Protection Agency, 2014). The natural landscape of Sierra Leone is also diverse comprising of lowland rainforest, mountain forest, freshwater swamps, mangrove/coastal and marine ecosystems and all of these landscapes are further broadly grouped into four main relief regions; coastline, interior lowland plains, interior plateau and mountains (Blinker, 2006; Environmental Protection Agency, 2014). The current status and potential of biodiversity is diminishing rapidly primarily due to anthropogenic activities.

1.5 Motivation for choice of study countries

The choice of Ghana and Sierra Leone for this study on the traditional medicinal use of pangolins was influenced by the high dependence of people on traditional medicine in both countries. In Ghana, it is estimated that 80% of the population depend exclusively on traditional medicine for their healthcare needs (WHO, 2001; WHO, 2002; Abel & Busia,

2005; Dove, 2010; Asante & Avornyo, 2013). Traditional medical practitioners form the backbone of Ghana’s healthcare delivery system with over 100 000 traditional medicine practitioners uniformly distributed nationally making them more accessible to the public

(WHO, 2001). Although Ghana’s healthcare system is well developed, people still use and rely heavily on the traditional medicine system (Sato, 2012). Most often, indigenous belief systems attribute illnesses to spirituality which is considered to be intrinsic to the Ghanaian cultural concepts of health and illness (Twumasi, 1979; Tabi, Powell & Hodnicki, 2006).

In Sierra Leone, up to 90% of the population rely on traditional medicine (Ministry of Health

& Sanitation, 2009; Shackman & Price, 2013) as the weak formal health institutions in this country may also be contributing significantly to this high reliance besides the strong traditional cultural affinities. The relatively recent civil war resulted in many formal

7 healthcare facilities being destroyed with the majority of health professionals leaving the country due to fear of being persecuted resulting in an acute shortage of human resources that is still pertinent till date (Desai, 2010). The prevailing weak formal health institutions have subsequently given credence to the traditional (informal) institutions, such as traditional medicinal practitioners who are now serving the needs of local communities.

The curative value of wildlife is recognized and valued by many people, who strongly rely on traditional medicine for their healthcare needs (Weiss, 1947; Ntiamoa-Baidu, 1987; Adeola,

1992; Anageletti et al., 1992; WHO, 2002; Lev, 2006). In addition, it has been documented that the use of whole, parts or products of animal species are utilized for the treatment of a wide range of human ailments in Ghana (Ntiamoa-Baidu, 1997; Dove, 2010; Insoll, 2011) and in Sierra Leone (Hanson-Alp et al. 2003; Awoyemi, 2014). However, detailed information about the use of specifically pangolins for medicinal purposes has not been documented in either country.

Ghana was chosen for the bushmeat study as it has a long history of trade in bushmeat

(Grubb et al., 1998) with records of trading in bushmeat dating back to the fifteenth century when De Marees chronicled smoked game being traded over long distances across Ghana

(Cowlishaw, Mendelson & Rowcliffe, 2004). In addition, bushmeat has played an important role in the economy of Ghana with Asibey (1977) suggesting that the growth of the cocoa industry, which is the primary export commodity of the country, would not have been possible without bushmeat supporting smallholder farmers as a source of food and cash income. In rural communities, bushmeat is still considered as one of the forest’s most valuable food products and an important component of their livelihoods (Ntiamoa-Baidu

1997; Crookes et al., 2007).

The bushmeat trade has been highly commercialized in recent years supplying both households within the rural community as well as urban areas (Brashares, Arcese & Sam,

2001). As estimated in 1998 that 385 000 tonnes of bushmeat are harvested each year in

Ghana (US$350 million) and 92 000 tonnes are marketed (US$83 million), with 60% of all sales taking place in urban areas (Ntiamoa-Baidu, 1998). In Ghana, severe depletion of mammals as a result of bushmeat hunting has contributed to the rapid decline in the populations of 41 mammal species since the 1970s (Brashares, Arcese & Sam, 2001).

Pangolins, which are often hunted, was ranked among 11 of the most preferred wild animal species for bushmeat in Ghana (Conservation International-Ghana, 2002). Yet, no study has been conducted outside major bushmeat market surveys to determine the extent of the trade on pangolins.

1.6 Thesis structure

Chapter 1 of this thesis provides an overview, motivation, objectives and background on study countries including a motivation for choosing the countries. Chapter 2 presents a general literature review of pangolin species with a focus on African pangolins. Chapters 3 and 4 address the medicinal use of pangolins in Sierra Leone and Ghana, respectively.

Chapter 5 investigates the extent of the pangolin bushmeat trade in Ghana while the hunter’s local ecological knowledge (LEK) of pangolins is discussed in Chapter 6. Chapter 7 brings together the key findings of the study with an emphasis on practical policy and future research recommendations. Chapters 3, 4 and 5 have already been published in Journal of

Ethnobiology and Ethnomedicine, PLOS One and Human Ecology, respectively.

CHAPTER 2

GENERAL LITERATURE REVIEW

2.1 General morphological characteristics of pangolins

Pangolins are a unique group of placental mammals that are covered in keratinised epidermal scales (Kingdon, 1971; Doran & Allbrook, 1973; Hoyt, 1987; Macdonald, 2001; Botha &

Gaudin 2007; Gaudin, Emry & Wible, 2009; Gaubert, 2011; Kingdon & Hoffman, 2013).

Indeed, pangolins are the only living mammals to have developed nail-like structures outside the digits region (Gaubert, 2011) that cover the entire body with exception of the underbelly.

They are also known as scaly anteaters because they are adapted to a myrmecophagous lifestyle, specialized for feeding only on ants and termites (Kingdon, 1971; Macdonald, 2001;

Botha & Gaudin, 2007; Lim & Ng, 2007; Akpona, Djagoun & Sinsin, 2008; Gaubert, 2011;

Kingdon & Hoffman, 2013; Challender, Waterman & Baillie, 2014). These animals have an exceptionally long sticky tongue that extend from the oral cavity, through the neck and thorax, to the abdomen which is rapidly protruded and withdrawn for capturing insects

(Herklots, 1937; Kingdon, 1971; Doran & Allbrook, 1973; Hoyt, 1987; Chan, 1995; Gaubert,

2011; Kingdon & Hoffman, 2013).

When threatened, their defensive strategy is to curl into a tight ball pulling its tail tightly over its face and belly to protect non-scaled parts (Kingdon, 1971; Hoyt, 1987; Bräutigam et al.,

1994; Gaubert, 2011; Kingdon & Hoffman, 2013). The name pangolin is actually derived from the Malayan word ‘pen-guling’ which means the ‘roller’ (Hoyt, 1987; Yang et al., 2007;

Gaubert, 2011).

Pangolins are secretive animals being mostly solitary and nocturnal, resting in their burrows or hollows for most part of the day till their foraging activities start late in the afternoon, at dusk or at night (Kingdon, 1971; Haltenorth & Diller, 1980; Bräutigam et al., 1994;

Macdonald, 2001; Gaubert, 2011; Kingdon & Hoffman, 2013). Their ability to store large quantities of body fat makes it possible for them to forego foraging for several days which contribute to their elusiveness (Gaubert, 2011). There is usually a loose bond between males and females with individuals remaining solitary in their well-defined home ranges except when coming together for short periods during mating (Kingdon, 1971; Haltenorth & Diller,

1980; Kingdon & Hoffman, 2013). Typically, a single young is born after a gestation period of 130-150 days (Kingdon, 1971; Sodeinde & Adedipe, 1994; Gaubert, 2011; Ganguly, 2013) which makes them more susceptible to severe population declines from hunting pressure as slower-breeding species are more at risk from extinction as such species are less resilient to increased mortality from hunting (Duncan, Blackburn & Worthy, 2002; Johnson, 2002; Price

& Gittleman, 2007; Fa & Brown, 2009).

2. 2 Taxonomy and general characteristics of African pangolins

The eight extant species of pangolins are equally distributed in Africa and Asia and are allocated to the class Mammalia, order Pholidota and to the single family Manidae (Botha &

Gaudin, 2007; Gaudin, Emry & Wible, 2009; Gaubert, 2011; Kingdon & Hoffman, 2013).

The name Pholidota comes from the Greek words pholis or pholidos, meaning horny scale

(Kingdon & Hoffman, 2013) while the names Manidae and Manis are from the Latin word manes, which means spirit of the dead or ghost, thus referring to the pangolin’s quite nocturnal habits (Gaubert, 2011). The extinct forms of Pholidota are generally thought of as being morphologically and anatomically more primitive in various respects than the living

11 taxa, but there is no consensus with regards to the phylogeny amongst the extant species and among the extant and extinct taxa (Gaudin & Wible, 1999; Gaudin, Emry & Wible, 2009).

Based upon a comprehensive analysis of 395 osteological characteristics of the skull and postcranial skeleton (Figure 2.1), Gaudin, Emry and Wible (2009) divided the extant species into three well-supported monophyletic genera: Manis for the Asian pangolins, Phataginus for the African tree pangolin and Smutsia for the African ground pangolins.

The two arboreal species Phataginus tricuspis and P. tetradactyla have a slight body with a tail longer than its head and body, thin scales as well as light body weight with the ventral terminus of the tail having a skin pad rather than scales in contrast to the ground-dwelling species Smutsia temminckii and S. gigantea (Kingdon & Hoffman, 2013). The ground pangolins are characterised by a stout body, short and stumpy hind legs, a tail shorter than the head and body length (Kingdon & Hoffman, 2013). Scales cover the outside of the fore and hind limbs as well as ventral aspects of the tail terminus of the ground pangolins (Kingdon &

Hoffman, 2013). Earlier morphological characteristics in Pholidota indicate that the two

African arboreal pangolins share more derived similarities than do the African ground pangolins (Gaudin & Wible, 1999).

Figure 2.1: Phylogeny of Pholidota based on PAUP

(Phylogenetic Analysis Using Parsimony) analysis of 395 osteological characters in 15 ingroup taxa, including seven of the eight extant pangolin species, five fossil pangolins,

Eurotamandua joresi, and two metacheiromyid palaeanodont genera, Palaeanodon and

Metacheiromys (Adapted from Gaudin, Emry & Wible, 2009).

2.2.1 White-bellied pangolin (P. tricuspis)

The white-bellied pangolin (Plate 2.1) has a slender tail that is about 1.5 times longer than the head and body (Kingdon, 1971; Haltenorth & Diller, 1980; Kingdon & Hoffman, 2013) with

34-37 marginal scales on the tail (Kingdon & Hoffman, 2013). There are between 19-22 rows of striated scales on the body that is generally small, very numerous, light-weight, and tight fitting and covers the neck, back limbs and extends to the toes of the hindlimbs but ends at elbows of the forelimbs (Kingdon & Hoffman, 2013). Their scales are coloured uniformly from brownish-grey to rufous and yellowish brown (Gaubert, 2011).

Plate 2.1: White-bellied Pangolin (Photo credit: African Pangolin Working Group)

The belly has sparse white hairs while the limbs and face has thicker black hair (Kingdon,

1971; Kingdon & Hoffman, 2013). Underneath the tail is a naked pad that together with their

14 large curved claws is used to assist in clinging to branches, probing for support as well as balancing round lianas (Herklots, 1937; Kingdon, 1971; Haltenorth & Diller, 1980, Kingdon

& Hoffman, 2013). The white-bellied pangolin is commonly solitary and scent-oriented with all social contacts depending on scent and is also highly sensitive to sound and vibration

(Gaubert, 2011; Kingdon & Hoffman, 2013). White-bellied pangolin breeds continuously with virtually non-existent or very short period of inactivity between pregnancies (Kingdon &

Hoffman, 2013). Gestation period is estimated to be in the region of 150 days with a single young born (Gaubert, 2011; Kingdon & Hoffman, 2013).

2.2.2 Black-bellied pangolin (P. tetradactyla)

The long-tailed pangolin (Plate 2.2) is unique in being the mammal with the greatest number of tail vertebrae which represents a clear adaptation to a super-arboreal existence with the tail serving as a fifth limb that sustain the entire animal’s weight for sustained periods (Gaubert,

2011; Kingdon & Hoffman, 2013).

Plate 2.2: Black-bellied pangolin (Photo credit: African Pangolin Working Group)

The tail length is twice that of the head and body and has sharply pointed scales, especially along the margins of its flattened undersides with 44 marginal scales on the tail (Kingdon &

Hoffman, 2013). Scales cover the forehead, back, limbs and waist but are absent from the upper surface of the forefoot while the cheeks, throat underside and limbs are well covered in coarse black hair (Gaubert, 2011; Kingdon & Hoffman, 2013). Scales cover the forehead, back, limbs and waist but are absent from the upper surface of forefoot while the cheeks, throat underside and limbs are well covered in coarse black hair (Gaubert, 2011; Kingdon &

Hoffman, 2013). The body scales are larger, darker and less striated with conspicuous pale margins and also less numerous (10-13 rows on body) (Kingdon & Hoffman, 2013).

Breeding in the long tailed pangolin is seasonal and almost continuous as the female conceives again within 9-16 days of giving birth to a single young with a gestation period of about 140 days (Gaubert, 2011; Kingdon & Hoffman, 2013).

2.2.3 Giant ground pangolin (S. gigantea)

The giant ground pangolin (Plate 2.3) is the largest and heaviest of all living pangolin species

(Gaubert, 2011; Kingdon & Hoffman, 2013). The tail is shorter in length than head and body

(Gaubert, 2011). The body has (17+ rows) of overlapping scales of different size and shape that are arranged in conformity with an obliquely angled, linear grid, with the largest scales along the middle of the back, flanks, shoulders and thighs with scales on limbs graduated and modified to allow maximum flexibility without loss to the protective armament of the limbs

(Kingdon & Hoffman, 2013). 15-19 sharply angled pointed scales that interdigitate with large and smaller scales borders the outer margins of the tail (Kingdon & Hoffman, 2013). The scales are uniformly coloured form beige to grey-brown (Gaubert, 2011). Hindlimb feet have

16 five toes that are short and blunt and aligned along the front of graviportal manner similar to elephant-like to support their weight (Kingdon, 1971; Kingdon & Hoffman, 2013).

Plate 2.3: Giant ground pangolin (Photo credit: Kes and Fraser Smith)

Social behaviour is governed by scent for both sexes where anal glands are used for marking territories. The giant ground pangolins are usually solitary animals; young ones usually accompany their mother until a new one is born (Kingdon & Hoffman, 2013). Breeding occurs throughout the year with peaks in some regions (Kingdon & Hoffman, 2013) and the gestation period is estimated at 150 days (Gaubert, 2011).

2.2.4 The Temminck’s ground pangolin (S. temminckii)

The most prominent feature of the ground pangolin (Plate 2.4) is their armour of hard, sharp, pantile-like overlapping scales that constitute one-third of its body weight (Kingdon, 1971,

Kingdon & Hoffman, 2013) where adult males are generally twice as heavy as females

(Gaubert, 2011).

Plate 2.4: Temminck’s ground pangolin (Photo credit: African Pangolin Working Group)

With the exception of the throat, belly and insides of the limbs that are sparsely covered with short hairs, the entire body is covered with scales (11-13 rows, and 11-13 scales on the tail margin) (Kingdon & Hoffman, 2013). Scales on the body, tail and forelimbs point to the posterior whereas those of the hindlimbs point down (Kingdon & Hoffman, 2013). Ground pangolins live a solitary existence besides coming together to mate and have a gestation period of about 140 days (Kingdon, 1971; Kingdon & Hoffman, 2013).

2.3 Habitat and distribution

Pangolins are distributed across a wide range of habitats ranging from tropical and sub- tropical forests, with habitat spectrum ranging from riparian and swamp forest, primary forest, dry woodland, savannahs with dense undergrowth regions, as well as artificial and modified habitats such as oil palm and rubber plantations (Gaubert, 2011; Kingdon &

Hoffman, 2013, Challender, Waterman & Baillie, 2014). Availability of ant and termites, water sources as well as favourable undergrowth to provide shelter for terrestrial species, and large trees or logs for arboreal species, determine the presence of pangolins (Gaubert, 2011).

The distribution of the four African pangolin species is presented in Figure 2.2.

Figure 2.2: Distribution of the four African pangolin species (Adapted from Challender,

Waterman & Baillie, 2014)

Phataginus tricuspis is endemic to Africa and is distributed across west and central Africa ranging from Guinea in West Africa through much of central Africa to the southernmost boundaries of SW Kenya, extreme W Tanzania, NW Zambia, and N Angola (Gaubert, 2011;

Kingdon & Hoffman, 2013). Their habitat includes patches of rainforest and savanna woodlands and is also adapted to modified human landscapes such as oil palm groves, teak plantations, fallows and secondary rainforest (Akpona, Djagoun & Sinsin, 2008; Gaubert,

2011; Kingdon & Hoffman, 2013). Phataginus tetradactyla on the other hand shows a marked preference for swamps and flooded forest areas (Angelici, Egbide & Akani, 2001;

Gaubert, 2011; Kingdon & Hoffman, 2013). Due to their association with riparian and permanent water bodies, they are considered to be semi-aquatic (Gaubert, 2011). Phataginus tetradactyla occurs from Sierra Leone to SW Ghana with an apparent gap in distribution until

W Nigeria, then eastwards through S Cameroon and much of the Congo basin forest block into Uganda (Angelici, Egbide & Akani, 2001; Gaubert, 2011; Kingdon & Hoffman, 2013).

Giant ground pangolin (S. gigantea) are found along riparian forest, rainforest, savannah- forest mosaics as well as high-rainfall secondary grasslands where it can shelter in thick- covered termitaries (Kingdon, 1971; Gaubert, 2011; Kingdon & Hoffman, 2013). They are distributed from Senegal to Ghana with apparent gap in distribution from Dahomey Gap and

Nigeria until the rainforest block in Cameroon and the Congo basin forest block to W Kenya,

Tanzania and Uganda (Kingdon, 1971; Gaubert, 2011; Kingdon & Hoffman, 2013). The

Temminck’s ground pangolin (S. temminckii), does not inhabit forest areas, rather it prefers savannas and woodlands in low lying regions often with dense undergrowth as well as flood- plain grasslands and sandveld that may reach an altitude of up to 1700 m (Gaubert, 2011;

Kingdon & Hoffman, 2013). Their range of distribution extend from E Chad through N of

Central African Republic to extreme W Ethiopia, then south through most of E and W part of southern Africa to South Africa (Gaubert, 2011; Kingdon & Hoffman, 2013; Challender,

Waterman & Baillie, 2014).

The distribution, population densities as well as habitat preferences for P. tricuspis, P. tetradactyla and S. gigantea are all estimates at best as no empirical ecological studies or comprehensive distributions records have been published for these African pangolins.

2.4 Conservation status and threats

All four African pangolin species are listed on Appendix II of CITES (Convention on

International Trade in Endangered Species of Wild Fauna and Flora) that requires close monitoring of their trade (Challender, Waterman & Baillie, 2014). The African Convention on Nature and Natural Resources list pangolins under Class B of protected species that gives it total protection from being hunted, killed, captured or collected unless under special permission by a competent authority (Organisation of African Unity, 1968). In addition, national laws in most African countries forbid the hunting and trade of pangolins in its natural ranges. At the moment, all four African species have been upgraded to Vulnerable in the recently revised IUCN Red Data List of Endangered Species (IUCN, 2014).

Despite both national and international conventions and laws that protect pangolins, they are consistently hunted for bushmeat as well as traditional medicinal purposes in all countries in

Africa where they occur and more recently traded in large volumes to Asia (Challender &

Hywood, 2012). The use of pangolins for traditional medicinal purposes is common in Africa

(Brautigam et al., 1994; Gaubert, 2011; Kingdon & Hoffman, 2013; Challender, Waterman &

Baillie, 2014; Soewu & Sodeinde, 2015). Throughout southern Africa (Cunningham &

Zondi, 1991; Marshall, 1998, Anchors, 2002; Challender & Hywood, 2012; Setlalekgomo,

2014), west Africa (Sodeinde & Adedipe, 1994; Sodeinde & Soewu, 1999; Akpona, Djagoun

& Sinsin, 2008; Soewu & Ayodele 2009; Soewu & Adekanola, 2011), central Africa

(Douglas 1957; 1990) and eastern Africa (Wright 1954; Marshall, 1998; Walsh, 1996, 2007), pangolins form an import part in the traditional medicine, rituals and religious symbolism of people.

Also, bushmeat surveys in Africa showed that pangolins are among the mammals consistently hunted and most preferred wild animal species (Martin, 1983; Anadu, Elamah &

Oates, 1988; Bräutigam et al., 1994; Sodeinde & Adedipe, 1994; Njiforti, 1996; Caspary,

1999; Fa & Gracía Yuste, 2001; Conservation International-Ghana, 2002; Fa et al., 2002; Fa et al., 2006; Crookes et al., 2007; Foerster et al., 2012; Gaubert, 2011; Bene, Gamys &

Dufour, 2013; African Pangolin Working Group, 2014; Soewu & Sodeinde, 2015). In Nigeria for instance, due to the expensive nature of pangolin meat, it is not a delicacy of choice but somehow a preserve for the rich because it is beyond the purchasing power of most ordinary people (Sodeinde & Adedipe, 1994; Gaubert, 2011; Soewu & Sodeinde, 2015).

Pangolins have symbolic importance, occupying a special place in the beliefs and rituals of some tribes in Africa. For example, among the Shona people of Zimbabwe, community residents give captured pangolins to chiefs, headmen, and sangomas in the belief they will bring protection, blessings, and well-being (Challender & Hywood, 2012). This animal also plays significant roles in the religions and rituals of some cultures and tribes, such as the

Hehe and Sangu of Tanzania and the Lele in the Democratic Republic of Congo (Walsh,

2007; Douglas, 1957). In some cultures, pangolin parts are worn on the body, such as among the Dzimbabwe of Zimbabwe who use pangolin designs on cloth to signify bravery and among chiefs in Nigeria, who wear attire with pangolin scales for protection from spirits

(Picton & Mack, 1989; Manwa & Ndamba 2011).

Considering the growing evidence of potential intercontinental trade in whole or body parts of pangolins between Africa and Asia (Cota-Larson, 2014), a zero trade quota for African pangolin species is recommended to ban all international trade. A zero trade quota is currently in place for Asian pangolin species (Allan et al., 2000). Also, the upgrade of

African pangolin species from Appendix II (limited trade) to Appendix I (no trade) needs to be critically evaluated and considered by CITES considering the current levels of harvest and international trade in pangolins and their body parts from the African continent to Asia.

CHAPTER 3

ETHNOMEDICINAL USE OF AFRICAN PANGOLINS BY TRADITIONAL

MEDICAL PRACTITIONERS IN SIERRA LEONE

3.1 Introduction

Traditional medicine dominates medical systems available to millions of individuals and remains the main, if not the only, source of medical care for the majority of people in the developing world (WHO, 2002; WHO, 2010a; Renckens & Dorlo, 2013). Animal-based remedies constitute an integral part of African traditional medicine both in rural and urban areas. An estimated 80% of the continent’s population depend on traditional medicine for their healthcare needs (Bodeker & Kronenberg, 2002; WHO, 2010a; Renckens & Dorlo,

2013). The people of Sierra Leone are no exception to this. The majority of the population of

Sierra Leone depend on traditional medicine to meet their healthcare needs (Ministry of

Health and Sanitation, 2009). Some 90% of deliveries at community level are attended by traditional birth attendants who are an integral component of traditional medical practice

(Ministry of Health & Sanitation, 2009). Shackman and Price (2013) also found that 90% of patients with mental health problems have received treatment from traditional healers in the

Northern Province of Sierra Leone. Indeed, traditional medicine is the first level of contact for most Sierra Leoneans due to inadequate healthcare facilities and affordability when these are available.

Traditional medical practitioners are highly dependent on harvesting from the biodiversity, and primary ingredients used by the traditional healers are wild animals, plant species and

24 mineral resources for the preparation of their therapeutic remedies for their patients (WHO,

2002; Kang & Phipps, 2003; Alves & Rosa, 2006). Animals have been documented as a source of medicine throughout human history. According to Weiss (1947), Anageletti et al.,

(1992), Lev (2006) Alves and Alves (2011), Alves and Souto (2011), animal-based medicines have been used since time immemorial. Most Africans attach special magical healing power to wild animals and their by-products used in traditional medicine (Adeola, 1992; Bräutigam et al., 1994; Marshall, 1998; Soewu & Ayodele, 2009; Alves, Souto & Barboza, 2010; Soewu

& Adekanola, 2011; Whiting, Williams & Hibbitts, 2011; Djagoun et al., 2013).

A mammal that has long been used for traditional medicinal purposes throughout Africa is the pangolin (Bräutigam et al., 1994; Sodeinde & Adedipe, 1994; Marshall, 1998; Sodeinde

& Soewu, 1999; Akpona, Djagoun & Sinsin, 2008; Soewu & Ayodele, 2009; Soewu &

Adekanola, 2011; Challender & Hywood, 2012; Soewu, Bakare & Ayodele, 2012) and also traditional medicinal systems in Asia (Chakravorty, Meyer-Rochow & Ghosh, 2011;

Chakkaravarthy, 2012; Kaspal et al., 2012). Pangolins or scaly anteaters belong to the order

Pholidota (Gaudin, Emry & Wible, 2009). They are covered with keratinous scales and have adapted to a specialised diet of ants and termites (Bräutigam et al., 1994; Kingdon, 1971; Lim

& Ng, 2007; Ganguly, 2013). They feed by burrowing with their claws adapted for raiding ant and termite mounds, aided by their highly modified elongated and sticky tongue specialised for consuming ants and termites (Kingdon, 1971; Lim & Ng, 2007; Ganguly,

2013). They are usually solitary and inhabit burrows or inside tree holes, and have a very slow reproduction rate (Kingdon, 1971; Ganguly, 2013). When threatened, they curl their body up like a ball in a defensive posture (Bräutigam et al., 1994; Ganguly, 2013).

All extant species of pangolin (four Asian species and four African species) are listed in

Appendix II of CITES. The black-bellied pangolin (Phataginus tetradactyla), white-bellied pangolin (Phataginus tricuspis) and the giant ground pangolin (Smutsia gigantea) are distributed throughout Sierra Leone (Challender, Waterman & Baillie, 2014). They occur mainly in forests and forest mosaics in moist and semi-deciduous forest habitat types. No previous studies have investigated the use of pangolins by traditional medical practitioners in

Sierra Leone and this is the first attempt to document the use of whole or parts of pangolins in the treatment of human-related diseases. In addition, this study investigates implications of pangolin use by traditional medical practitioners on the conservation status and potential threat to African pangolin biodiversity.

3.2 Materials and methods

3.2.1 Study site

The study was conducted in the Bombali district (9°20′N and 12°15′W) of Sierra Leone

(Figure 3.1). This district has a human population of 408,390 (Statistics Sierra Leone, 2004) and occupies a total area of 7 985 km2 (Bombali District Council, 2013). The district shares borders with the Republic of Guinea to the north, Port Loko and Kambia districts to the west,

Tonkolili district to the south and Koinadugu district to the east. Ethnically, the Temne and

Limba form the largest ethnic groups in Bombali district. Makeni is the headquarters and largest town in Bombali district. The Bombali district was chosen for this study because it is reported by the Justice and Peace and Human Rights Commission (2008) as having the poorest level of health services in Sierra Leone. The Development Assistance Coordinating

Office also classified Bombali district as the worst in secondary and primary healthcare

26 services when compared with other districts nationwide and, as a result, the inhabitants of

Bombali district depend heavily on traditional medical practitioners for their medical needs

(Shackman & Price, 2013).

Figure 3.1: Map of Africa indicating Sierra Leone and the study district of Bombali

For the purposes of this study TMP is referred to those people who are considered to be healers by the district Traditional Healers Association by virtue of their membership with the association.

3.2.2 Ethics Statement

This study was approved by the ethics committee of the Tshwane University of Technology

(REC Ref #: REC2013/05/008) and written informed consent was obtained from all participants interviewed.

3.2.3 Data collection

Ethnozoological data on medicinal use of pangolins was collected using semi-structured interviews held between the months of October to November 2013. During the first contacts with the local population, a meeting was held with the local tribal leader to explain the research and to obtain informed consent to conduct the study. The local tribal leader then introduced the researcher to the chairman of the local association of traditional healers. The objective of the research was explained to the chairman, who called a meeting of the association members to explain the project to them. The sampling process was purposeful with participants intentionally selected because they could provide the information about the issues identified as important to this study (Babbie, 2001). Of the 100 traditional medical practitioners requested to participate in this study, 98 members confirmed that they are using or have used whole or parts of pangolins in their remedies. Of these, 63 agreed to participate in this study with informed consent. Participants were made aware of their rights to decide to either voluntarily participate in the study or decline.

Semi-structured interviews were conducted to obtain information from respondents. The interview questions focused on the interviewees’ knowledge of the uses for pangolin parts or whole pangolins for medicinal purposes to cure or alleviate a particular medical ailment or set of ailments. Verbal prompts and probes were used to motivate informants and elicit information from them. The pace and direction of the interviews were dictated by the participants. Participants were shown photographs of the three African pangolin species distributed in Sierra Leone. The key questions that traditional medical practitioners were asked were: do you know the animal called pangolin (participants were requested to provide the local name) and do you know whether it serves as medicine? In the semi-structured

28 interviews, the traditional medical practitioners (interviewees) were requested to name particular species of pangolin and their parts used as medicine, the ailments for which that body part was prescribed and how the animals were obtained. The diseases and or conditions were scored in the appropriate category using the International Statistical Classification of

Diseases and Related Health Problems (ICD-10:2010). Traditional medical practitioners were also questioned on how this knowledge was acquired. All interviews were conducted in Krio

English language which is the most widely spoken language in Sierra Leone, with a local

Sierra Leonean translator translating if the interviewee did not understand certain aspects of the Krio English language. Demographic data of traditional medicinal practitioners were also collected.

3.3 Data analysis

Three quantitative value indices: Use values (UV), informant agreement ratio (IAR) and use agreement value (UAV) were calculated.

3.3.1 Use Value (UV)

The use value (UV) for each pangolin part was calculated employing a formula modified from Albuquerque et al. (2006), which uses animal parts instead of the whole individual. This approach is based on a quantitative method to demonstrate the importance of species parts given by a local population (Alves et al., 2012). The UV of each pangolin part mentioned was calculated using the formula:

∑ 푈푝 UV = 푛

29 where: Up = the number of uses mentioned by each informant for a given pangolin part, n = the total number of informants (Rossato, Leitão-Filho & Begossi, 1999; Albuquerque et al., 2006).

3.3.2 Informant Agreement Ratio (IAR)

The Informant Agreement Ratio (IAR) was used to measure the consensus level among informants for pangolin body part in the treatment of human ailments. The original formula proposed by Trotter and Logan (1986) was interpreted as follows:

푛푟 − 푛푐 퐼퐴푅 = 푛푟 − 1

where nr is the total number of medicinal responses registered for pangolin body part and nc is the number of disease categories that are treated with this body part. The number of disease categories (nc) was calculated as the number of the International Classification of Diseases

(ICD) categories (Version 10) (ICD-10 Version, 2010) that informants claimed to treat.

Sixteen ICD categories were identified but spiritual ailments were added because it plays an important role as causes of diseases in African folk health systems. The total number of ICD categories in this study was 17. The IAR of a medicinal part varies between 0 (when the number of health conditions treated equals the number of medicinal responses) and 1

(whereby all participants agree upon the exclusive use of the part for a particular health condition).

3.3.3 Use Agreement Value (UAV)

According to Thomas et al. (2009) this index provides a valid and easily derived estimation of a medicinal resources cultural significance. Following the suggestions of Thomas et al.

(2009), but using UV instead of Quality Use Value (QUV), the use agreement value (UAV) was defined as follows:

푈퐴푉 = 푈푉 × 퐼퐴푅

where UV is the use value of body part and IAR is the informant agreement ratio of a particular body part.

3.4 Results

Regarding gender of participants, 90% (n = 57) were males and 10% (n = 6) were females.

With regard to the age of participants, 37% (n = 23) were above 60 years, and 2% (n = 1),

14% (n = 9) and 48% (n = 30) were between 31–40, 41–50 and 51–60 years old, respectively.

Regarding the number of years of practice, 68% (n = 43) had practised for more than 20 years, 30% (n = 19) between 16–20 years and 2% (n = 1) between 11–15 years. With regard to formal education, 41% (n = 26) of the interviewees were illiterate, 57% (n = 36) had attended school but their education was below secondary level and 2% (n = 1) had attended school above secondary level. All the interviewees classified themselves as full-time traditional medical practitioners.

A total of 22 pangolin body parts were identified as being used and prescribed for the treatment of 59 diseases and ailments (Table 3.1). The scales of pangolins had the highest use report (UR), followed by oil meat, head and tail, respectively (Table 3.1). The throat, sex organs (both male and female) and liver had the lowest UR whereas the eyes, forefoot, thorax, toes and whole animal had the same UR. The scales, head, meat and tail were the body parts with the highest number of ICD category use reports, respectively (Table 3.1). The scales were used in 12 of the 17 ICD categories, the head and tail in 10 categories and meat in

9 categories.

Table 3.2 indicates the contribution of each ICD category to the total use value index (UV) of the 22 pangolin body parts used by the traditional healers. The highest UV of the scales was for spiritual ailments while the highest UV of tissue oil was for diseases of the skin and subcutaneous tissue. Diseases of the digestive system, symptoms, signs and abnormal clinical and laboratory findings not elsewhere classified, spiritual ailments and certain infectious and parasitic diseases received the highest UV for meat, head, tail and foot, respectively. The highest UV of the tongue was for diseases of the circulatory system while the highest UV of the bones was for diseases of the musculoskeletal system and connective tissue.

Table 3.3 indicates the contribution of each ICD category to the total informant agreement ratio (IAR) of the 22 pangolin body parts. The highest IAR value was recorded for the eyes, which was followed in a descending order by the oil, scale, bones, meat, tail and head. The eyes were only used under certain infectious and parasitic diseases category. The highest IAR value for the oil was linked to diseases of the skin and subcutaneous tissue. The highest IAR value for scales were linked to spiritual ailments and then followed in descending order by diseases of the skin and subcutaneous tissue and diseases of the musculoskeletal system and

32 connective tissue (Table 3.3). Pangolin bones prescribed for cures relating to diseases of the musculoskeletal system and connective tissue and had the highest IAR value while the highest IAR value of meat was for diseases of the digestive system. The highest IAR value for the tail and head were for cures or treatment relating to spiritual ailments. The claws, whole animal, toes, thorax, fore foot, throat, sex organ (both male and female) and liver recorded a zero IAR value as the number of use reports for each part in each use category is the same. This indicates that there was no agreement between informants on the use of these body parts.

Table 3.1: Use of pangolin body parts and the prescribed conditions treated, Use Report (UR) and International Classification of Diseases (ICD) categories

Parts Conditions treated Use ICD Categories report Scales Skin disease, impotence, infertility, broken ribs, stomach diseases, inflammation of the navel, 70 12 bulletproof, cutlassproof, athlete's foot, claw hand, nail disorders, healing premature babies, heel fissure, arthritis, rheumatism, epilepsy, ear infection, body pain, elephantiasis, waist pain, healing wound, skin rash, protection from witchcraft, broken bones, spiritual protection and skin scars Oil Skin rash, skin stretch marks, heel fissure, skin diseases, knee pain, skin scars, heart diseases, claw 27 5 hand, elephantiasis and body ache Meat Healing premature babies, stomach diseases, rheumatism, epilepsy, high blood pressure, for increasing 23 9 intelligence, body pain, common childhood diseases, convulsion and anaemia Head Infertility headache, antidote for poison, skin diseases, mental illness, toothache, heart disease, 21 10 paralysis, hernia and claw hand Tail Impotence, spiritual protection, Apollo (acute haemorrhagic conjunctivitis), paralysis, claw hand, 20 10 convulsion, fainting, stomach diseases, protection against snake bite, curse sting from scorpion, waist pain, elephantiasis and heel fissure Foot Heel fissure, back pain, elephantiasis, athlete's foot and broken bones 7 4 Tongue Rheumatism, stop/control bleeding, mental illness, piles and fainting 7 4 Bones Skin scars, healing wounds, stiffness of joints, rheumatism and joint pains 7 3 Blood Healing wounds, elephantiasis, rheumatism, stomach diseases, heart diseases and protection against 7 6 witchcraft

Parts Conditions treated Use ICD Categories report Male sex organ Hernia, headache, elephantiasis, athlete's foot, infertility and impotence 6 5 Intestines Stomach diseases, headache and for good luck 5 3 Claws Protection from witchcraft, skin stretch marks, asthma and heart burn 4 4 Brain Heart diseases, mental illness and stomach diseases 4 3 Heart Stomach diseases and heart diseases 3 2 Whole animal Leprosy and invisibility 2 2 Toes Apollo and epilepsy 2 2 Thorax Chest pain and broken ribs 2 2 Forefoot Impotence and elephantiasis 2 2 Eyes Apollo 2 1 Throat Goitre 1 1 Sex organ (both male Infertility 1 1 and female) Liver Asthma 1 1

Table 3.2: Use Value (UV) of pangolin body parts for each International Classification of Diseases (ICD) category

International Classification of Diseases (ICD) categories Total Parts 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 UV Scales 0.063 0.032 0.016 0.016 0.032 0.206 0.143 0.032 0.016 0.079 0.079 0.397 1.111 Oil 0.016 0.016 0.238 0.079 0.079 0.429 Meat 0.016 0.016 0.032 0.048 0.143 0.016 0.063 0.016 0.016 0.365 Head 0.048 0.016 0.016 0.048 0.016 0.016 0.032 0.111 0.016 0.016 0.333 Tail 0.048 0.016 0.032 0.016 0.016 0.032 0.016 0.032 0.016 0.095 0.317 Foot 0.048 0.032 0.016 0.016 0.111 Tongue 0.016 0.048 0.032 0.016 0.111 Bones 0.016 0.063 0.032 0.111 Blood 0.016 0.016 0.016 0.016 0.016 0.032 0.111 Male sex 0.032 0.016 0.016 0.016 0.016 0.095 organ Intestines 0.048 0.016 0.016 0.079 Claws 0.016 0.016 0.016 0.016 0.063 Brain 0.032 0.016 0.016 0.063 Heart 0.016 0.032 0.048 Whole 0.016 0.016 0.032 animal Toes 0.016 0.016 0.032 Thorax 0.016 0.016 0.032 Forefoot 0.016 0.016 0.032

International Classification of Diseases (ICD) categories Total Parts 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 UV Eyes 0.032 0.032 Throat 0.016 0.016 Sex organ 0.016 0.016 (both male and female) Liver 0.016 0.016 Codes for ICD categories: 1=Certain infectious and parasitic diseases, 2=Diseases of the blood and blood-forming organs and certain disorders involving the immune mechanism, 3=Endocrine, nutritional and metabolic diseases, 4=Mental and behavioural disorders, 5=Diseases of the nervous system, 6=Diseases of the ear and mastoid process, 7=Diseases of the circulatory system, 8=Diseases of the respiratory system, 9=Diseases of the digestive system, 10=Diseases of the skin and subcutaneous tissue, 11=Diseases of the musculoskeletal system and connective tissue, 12=Diseases of the genitourinary system, 13=Certain conditions originating in the perinatal period, 14=Symptoms, signs and abnormal clinical and laboratory findings not elsewhere classified, 15=Injury, poisoning and certain other consequences of external causes, 16=Factors influencing health status and contact with health services, 17=Spiritual ailments

Table 3.3: Informant Agreement Ratio (IAR) of pangolin body parts for each International Classification of Diseases (ICD) category

International Classification of Diseases (ICD) categories Total Parts 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 IAR Scales 0.048 0.024 0.012 0.012 0.024 0.156 0.108 0.024 0.012 0.060 0.060 0.300 0.841 Oil 0.031 0.031 0.470 0.157 0.157 0.846 Meat 0.028 0.028 0.055 0.083 0.249 0.028 0.111 0.028 0.028 0.636 Head 0.079 0.026 0.026 0.079 0.026 0.026 0.052 0.183 0.026 0.026 0.550 Tail 0.079 0.026 0.053 0.026 0.026 0.053 0.026 0.053 0.026 0.158 0.579 Foot 0.214 0.143 0.071 0.071 0.500 Tongue 0.071 0.214 0.143 0.071 0.500 Bones 0.095 0.381 0.190 0.667 Blood 0.024 0.024 0.024 0.024 0.024 0.048 0.167 Male sex 0.067 0.000 0.033 0.033 0.033 0.033 0.200 organ Intestines 0.300 0.100 0.100 0.500 Claws 0.000 0.000 0.000 0.000 0.000 Brain 0.167 0.083 0.083 0.333 Heart 0.167 0.000 0.333 0.500 Whole 0.000 0.000 0.000 animal Toes 0.000 0.000 0.000 Thorax 0.000 0.000 0.000 Forefoot 0.000 0.000 0.000

International Classification of Diseases (ICD) categories Total Parts 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 IAR Eyes 1.000 1.000 Throat 0.000 0.000 Sex organ 0.000 0.000 (both male and female) Liver 0.000 0.000 Codes for ICD categories: 1=Certain infectious and parasitic diseases, 2=Diseases of the blood and blood-forming organs and certain disorders involving the immune mechanism, 3=Endocrine, nutritional and metabolic diseases, 4=Mental and behavioural disorders, 5=Diseases of the nervous system, 6=Diseases of the ear and mastoid process, 7=Diseases of the circulatory system, 8=Diseases of the respiratory system, 9=Diseases of the digestive system, 10=Diseases of the skin and subcutaneous tissue, 11=Diseases of the musculoskeletal system and connective tissue, 12=Diseases of the genitourinary system, 13=Certain conditions originating in the perinatal period, 14=Symptoms, signs and abnormal clinical and laboratory findings not elsewhere classified, 15=Injury, poisoning and certain other consequences of external causes, 16=Factors influencing health status and contact with health services, 17=Spiritual ailments

There were appreciable differences in body parts ranked according to the three indices (Table

3.4) where the ranking order varied depending on the index. The UV and UAV indices place scales at the highest rank followed by oil, meat, head and tail for both indices. This was not same for the IAR which ranked the eyes as the most important body part. The throat, sex organ (both male and female) and liver were the lowest in all indices.

Table 3.4: Evaluation of pangolin body parts using Use Value (UV), Informant Agreement

Ratio (IAR) and Use Agreement Value (UAV)

Indices Ranking Parts UV IAR UAV UV IAR UAV Scales 1.111 0.841 0.934 1 3 1 Oil 0.429 0.846 0.363 2 2 2 Meat 0.365 0.636 0.232 3 5 3 Head 0.333 0.550 0.183 4 6 4 Tail 0.317 0.526 0.167 5 7 5 Foot 0.111 0.500 0.056 6 8 7 Tongue 0.111 0.500 0.056 6 8 7 Bones 0.111 0.667 0.074 6 4 6 Blood 0.111 0.167 0.019 6 11 12 Male sex organ 0.095 0.200 0.019 7 10 12 Intestines 0.079 0.500 0.040 8 8 8 Claws 0.063 0.000 0.000 9 12 13 Brain 0.063 0.333 0.021 9 9 11 Heart 0.048 0.500 0.024 10 8 10 Whole animal 0.032 0.000 0.000 11 12 13 Toes 0.032 0.000 0.000 11 12 13 Thorax 0.032 0.000 0.000 11 12 13 Forefoot 0.032 0.000 0.000 11 12 13 Eyes 0.032 1.000 0.032 11 1 9 Throat 0.016 0.000 0.000 12 12 13 Sex organ (both male and female) 0.016 0.000 0.000 12 12 13 Liver 0.016 0.000 0.000 12 12 13

3.5 Discussion

3.5.1 Use value (UV)

High use values indicate that pangolin body parts are frequently used in traditional healing practices and hold a high level of importance as a source of treatment in patients by local traditional medical practitioners and healers (Alves & Rosa, 2006; Alves et al., 2012). The high UV for pangolin scales implies that the scales are extremely important to the traditional medical practitioners. Rossato, Leitão-Filho and Begossi (1999) state that a UV of more than

1 indicates that community members or TMPs use this resource for numerous medicinal ailments. The scales were found to be the most medicinally versatile body part, and were applied in 12 out of the 17 (71%) ICD categories. The high use of scales found in this study corroborates with findings by Bräutigam et al. (1994) in that a large portion of medical ailments are treated making use of pangolin scales. This was also found to be the case in the

Awori people of Nigeria (Soewu & Adekanola, 2011).

This study found scales to be very important in the treatment of spiritual ailments in addition to the preparation of charms, warding off evil spirits and witchcraft which has also been mentioned in previous studies (Bräutigam et al., 1994; Akpona, Djagoun & Sinsin, 2008;

Soewu & Ayodele, 2009; Soewu & Adekanola, 2011; Challender & Hywood, 2012).

Furthermore, the high UV of pangolin scales in treating diseases of the skin and subcutaneous tissue can be attributed the importance attached to pangolin scales by the traditional healers in

Sierra Leone. This study found a high use of pangolin scales for treating rheumatism which has also been mentioned in previous studies (Bräutigam et al., 1994; Akpona, Djagoun &

Sinsin, 2008; Soewu & Ayodele, 2009; Soewu & Adekanola, 2011) although they did not determine the level of knowledge among their respondents.

The use of pangolin oil in treating diseases has not been previously reported and the UV observed in this study is high and therefore is an indication that it is highly valued by the traditional medical practitioners as a source of medicine in Sierra Leone. Knowledge about pangolin oil as a therapeutic resource was mostly limited to diseases of the skin and subcutaneous tissue that had the highest UV among the five ICD categories. The oil is obtained by placing a pan beneath a pangolin while it is being smoked over a fire. Bräutigam et al. (1994) mentions that pangolin meat is less valued in terms of medicinal properties to other body parts, however, this study indicates that the meat was relatively important for the people of Sierra Leone ranking third in terms of its use value. Moreover, the therapeutic properties of the meat are quite specific with knowledge about the meat mostly limited to diseases of the digestive system.

The therapeutic properties of the tail was more limited to spiritual ailments and the relatively low UVs for feet, tongue, bones and blood can be attributed less frequent use by traditional medical practitioners than other body parts for treating ailments. Bones were prescribed primarily for treating musculoskeletal and connective tissue disorders but it has also been reported to treat rheumatism within Nigerian tribal communities (Soewu & Ayodele 2009;

Soewu &Adekanola 2011). The head was found to be medicinally versatile and is thus involved in treating different diseases under various ICD categories, but was more important to traditional medical practitioners and the local community for the treatment of ailments such as headache, skin rash, fainting (syncope), waist pain, body pain, back pain and body aches. This study found that the pangolin head was prescribed within 10 ICD categories, a

42 great deal more than was found in similar studies undertaken in Nigeria (Soewu & Ayodele,

2009; Soewu &Adekanola, 2011). Furthermore, the thorax and eyes have been reported as having a medicinal use in Nigeria and the tongue, heart and feet have also been used in the

Republic of Benin for the treatment of asthma, accelerated heart beating, normal growth and baby vigour (Akpona, Djagoun & Sinsin, 2008). Also, studies in Nigeria indicate the entire animal can be prescribed for invisibility which this study did not record in Sierra Leone. It is therefore likely that the prescriptive use of certain pangolin body parts varies between

African tribal communities and cultures across the species range.

3.5.2 Informant Agreement Ratio (IAR)

The IAR values are a reflection of the extent consensus about the use of pangolins in a community or among a group of people. High consensus is an indication that a particular pangolin part is preferred in the community for treatment of specific ailments (Gazzaneo,

Lucena & Albuquerque, 2005; Almeida et al., 2006; Alves & Rosa, 2006). Interestingly, the eyes and not the scales had the highest IAR value and are only used to remedy certain infectious and parasitic diseases. The high IAR for tissue oil and scales can be associated with the high importance and prescriptive use attached to it by the traditional healers.

According to Heinrich et al. (2009), a high consensus value indicates that the medicinal resource may be an important part of local cultural knowledge. As such, the high IAR for tissue oil to treat diseases of the skin and subcutaneous tissue can be said to be an important remedy within the cultural knowledge of traditional medical practitioners as it scored the highest IAR than all the other categories. Likewise, the high IAR for scales in the treatment of spiritual ailments which was the highest IAR for a single ICD category of any body part can be seen to play a large factor within traditional medical practitioners of Sierra Leone.

On the contrary, the low consensus values indicated for claws, whole animal, toes, thorax, fore foot, throat, sex organs and liver may be an indication that these body parts have fallen into disuse because of cultural adaptation or believed to be ineffective for treating conditions reported or may simply be of low cultural importance in traditional medicine. Even though a medical resource may be mentioned in traditional pharmacopoeia, this does not necessarily mean that it is perceived as an effective treatment of a condition or alleviating symptoms

(Thomas et al., 2009). This may be the case with regards body parts with low use values and informant agreement ratios and may be an indication that those parts are not effective in treating conditions or alleviating symptom although they occur in within this traditional pharmacopoeia.

One disease that was surprisingly not mentioned but that occurs in the study area and affects a large number of locals but not treated with pangolin parts is malaria. The selection and use of a resource for traditional medicinal purposes are usually based on culturally perceived effectiveness (Heinrich et al., 1998). The lack of effectiveness of pangolin body parts for the treatment of malaria may have accounted for its noticeable absence in the list of diseases mentioned by traditional medical practitioners.

3.5.3 Comparing different indices

Both the UV and IAR varied for different ICD categories. Thomas et al. (2009) attributes this variation to the idiosyncratic knowledge of most traditional healers resulting in low levels of consensus for use categories among practitioners. According to Thomas et al. (2009), the distribution of knowledge about traditional remedies follows a pattern whereby few remedies are known to almost everyone while most knowledge is idiosyncratic. All the TMPs

44 interviewed mentioned that they obtained their knowledge verbally from a family member

(mother, father, uncle and aunt). Thus their medicinal knowledge reflects knowledge acquired and accumulated over time and that it is likely to be family-specific or idiosyncratic in nature.

Based on the ranking of the indices, the scales, oil, meat, head, tail, foot, tongue and bones were the most widespread body parts used for medicinal purposes although their ranking varied depending on the chosen index. The combination of the number of use reports and the level of consensus between participants seems to provide a valid and easily derived estimate of cultural significant (Thomas et al., 2009) and, it can therefore be deduced that the culturally important pangolin body parts found in this study are those with high use agreement values. The scales had the largest average number of use reports and were used to treat more ICD categories than any other body part. It can therefore be argued, based on the index of use agreement value, that the cultural importance of pangolin scales in traditional pharmacopoeia is very high within Sierra Leone. The other culturally significant pangolin body parts used for medicinal purposes in descending order are oil, meat, head, tail, foot, tongue and bones.

3.6 Conservation implications

Undoubtedly, the high dependency on traditional medicine as well as high level of consensus among healers on the choice of body parts to be used in treating various ailments raises concern about the level of harvesting of pangolins for medicinal purposes in Sierra Leone.

All the significant body parts based on the UAV are used to cure culturally bound syndromes as well as diseases that have been identified as prevalent in Sierra Leone. Culture-bound syndromes or folk illness usually have no substituted or alternative remedies with healers

45 relying on what they are culturally familiar with. For instance, pangolin body parts used in the form of amulets and charms in the treatment of spiritual ailments cannot be substituted with another animal or provided for clinically. The belief systems may not provide an option for another alternative medicine, making sole reliance on pangolin body parts inevitable.

According to Costa-Neto (2004), cultural medical systems are often organised within cultural systems and the use of animals or parts thereof within these medical systems should be understood from a cultural perspective. Often, the effectiveness of traditional medicinal resources is not simply a consequence of their pharmacology but also stems from a cultural and traditional background and belief system of a tribe or community (Moerman, 2007).

This study has indicated that particular pangolin body parts, such as scales, have an important cultural medicinal value and are prescribed frequently within Sierra Leon. The harvest of pangolins is further increased by the high use values for treatment of diseases of the digestive system, diseases of the skin and subcutaneous tissue and diseases of the musculoskeletal system and connective tissue that have been identified as very prevalent in Sierra Leone by the WHO (2009, 2010b). Furthermore, none of the body parts used to treat conditions under these ICD categories can be obtained without killing the animal which further raises concerns about the impact of harvesting pressure on these animals. Also, there are no cultural taboos associated with the traditional medicinal use as well as harvesting of pangolins at any time of the year among traditional medical practitioners interviewed in Sierra Leone. Pangolins can subsequently be regarded as highly sought after for traditional medicinal practices and actively pursued or poached in this country. As such, an assessment of the cultural dimension of pangolin use in traditional medicine is critical for conservation efforts for the species. The actual levels of harvest or trade is not documented neither is the turn-over rates within bush meat markets or medical practitioner use in this country. Furthermore, the extent of

46 international trade, particularly towards Asia, is on the rise. Recently, two shipments of pangolin scales originating from East and West Africa, respectively, with a combined mass of

3.3 tonnes were intercepted in Hong Kong harbour by customs officials during May and June

2014 (Cota-Larson, 2014).

All three species of African pangolin occurring within Sierra Leone; black-bellied pangolin

(Phataginus tetradactyla), white-bellied pangolin (Phataginus tricuspis) and the giant ground pangolin (Smutsia gigantea) are listed on CITES Appendix II and can only be traded following a Non-Detriment Finding study that has been completed and logged. However, this has never been done for any of the African species. Furthermore, all three species have been up-listed as Vulnerable on the recently revised IUCN Red List (Challender, Waterman &

Baillie, 2014). All three pangolin species are protected under the Wildlife Conservation Act of 1972 in this country and offenders of a first conviction may be fined or sentenced with a prison term not exceeding six months, or both may apply. For a second and subsequent conviction a fine or a prison term not exceeding 12 months, or both, may be imposed.

However, this penalty is rarely imposed and in addition to the poor enforcement of conservation laws, as in most developing countries, it does not contribute to the conservation of pangolins.

Currently, there is little data that assesses the status and use of African species of pangolins when compared to Asian species. Alves, Rosa and Santana (2007) have identified the need to increase understanding of the biology and ecology of species commonly used as remedies to better assess the impact of harvesting them for medicinal or other purposes on their wild populations. This is critical for pangolins since all the species used by traditional medical practitioners in this study and studies elsewhere (Soewu & Ayodele, 2009; Soewu &

Adekanola, 2011) were harvested from the wild with no known record of captive breeding or domestication. Based on their habitat and prey requirements, reproductive rates, population distribution, degree of habitat alteration, levels of hunting pressure and medicinal value, all pangolin species are susceptible to extinction (Sodeinde & Adedipe, 1994; Challender,

Waterman & Baillie, 2014). High demand for pangolins from the wild may lead to a strong possibility of overexploitation through medicinal use, which requires an urgent ecological evaluation of the population in the wild. The impact of animal-based medicinal practices on wild populations therefore needs to be carefully assessed considering that preparation of most animal-based remedies requires killing of the animal.

Conservation efforts should therefore be aimed at educating traditional medical practitioners about the implications of their medical practices on wild populations. Traditional medical practitioners must be made aware that a decrease in medicinal wildlife not only affects biodiversity but will jeopardise their socioeconomic status since the raw materials they rely on to treat the patients will no longer be available. It is therefore imperative for them to ensure the continuous survival of these animals through sustainable utilization of wild populations.

3.7 Conclusion

Traditional medicine represents an alternative source of healthcare for most people in Sierra

Leone and knowledge about the medicinal properties of pangolins is very customary among the local people as well as traditional medical practitioners. This was evident in the high cultural and therapeutic importance associated with pangolin body parts. The folk culture of the people is the key factor in maintaining and driving the use of pangolins for therapeutic

48 purposes. The lack of enforcement of wildlife conservation laws is negatively affecting the sustainable harvesting of pangolins as it is currently very likely an over exploitation of a threatened and vulnerable species. Collaboration between conservation agencies and traditional medical practitioners through the involvement of the local community is necessary to prevent a population crash of three African pangolin species which will, in turn, have an impact on the cultural use of the species. Conservation efforts should therefore be aimed at increasing awareness among traditional medical practitioners and soliciting their support to ensure the success of conservation programmes and sustainable pangolin use. Further studies with regards the use of pangolins as therapeutic resources is necessary in other African countries to increase the understanding of the requirement for the species as a source of traditional medicine. In addition, there is a need to document the potential impact on the species with regards to local harvest levels.

CHAPTER 4

KNOWLEDGE AND USES OF AFRICAN PANGOLINS AS A SOURCE OF

TRADITIONAL MEDICINE IN GHANA

4.1 Introduction

It is currently estimated that 80% of Africa′s population uses traditional medicine (TM)

(WHO, 2002) either on its own or collectively with Western medicine (Dove, 2010). TM plays a very important complementary role in healthcare delivery systems in Ghana as between 70–80% of Ghanaians depend on TM for their primary healthcare needs (Abel &

Busia, 2005; Dove, 2010; Asante & Avornyo, 2013) and therefore it has a high level of cultural acceptability and use. Historically, TM was the only known default form of healthcare until the introduction of modern medicine by the British medical officers during the colonisation of the country (Twumasi, 1979). Although the majority of Ghanaians have embraced modern scientific medicine, indigenous health beliefs are commonly sought within urban and rural communities in this country (Tabi, Powell & Hodnicki, 2006) and is recognized by the government as a component of the healthcare delivery system where the

Traditional Medicine Practice Act (Act 575 of 2000) provides the legal framework for the practice of TM in Ghana. Compared to other countries in sub-Sahara Africa, Ghana’s TM system is relatively well established because it has been incorporated into the national health programmes and policies (Sato, 2012).

The use of whole, parts or products of animal species for the treatment of a wide range of human ailments in Ghana has been recorded (Ntiamoa-Baidu, 1997; Dove, 2010; Insoll,

2011) but only Ntiamoa-Baidu (1997) mentioned the use of scales of one of the tree pangolin

50 species for the treatment of cough in Ghana. The use of pangolins in traditional medicinal practices is of particular interest as it is well documented as being used within traditional medicinal systems in Asia (Gaski & Johnson, 1994; Kang & Phipps, 2003; Kaspal et al.,

2012; Chakkaravarthy, 2012) and as a source of traditional medicine in those parts of Africa where they occur (Bräutigam et al., 1994; Sodeinde & Adedipe, 1994; Marshall, 1998;

Sodeinde & Soewu, 1999; Akpona, Djagoun & Sinsin, 2008; Soewu & Ayodele, 2009;

Soewu & Adekanola, 2011; Challender & Hywood, 2012; Soewu, Bakare & Ayodele, 2012;

Chapter 3). However, the parts of the animal used and the ailments for which they are prescribed are unrecorded. In addition, it is unknown at what level these animals are regarded as an important source of cultural significance within traditional medical practices in Ghana.

There are three species of pangolin found in Ghana; black-bellied pangolin (Phataginus tetradactyla), white-bellied pangolin (Phataginus tricuspis) and the giant ground pangolin

(Smutsia gigantea) (Gaudin, Emry & Wible, 2009). As yet, no studies have been conducted investigating off-take or harvest levels, the prevalence of use and level of knowledge of pangolins for medicinal purposes among traditional healers in Ghana. Such information is essential in devising strategies for the conservation of pangolins. Therefore, the aim of this study was to determine the prevalent use of whole animals or body parts and the level of knowledge of pangolins as a medicinal resource among traditional healers in Ghana.

4.2 Materials and Methods

4.2.1 Study area

The study was conducted in the Kumasi Metropolitan area in the Ashanti Region of Ghana.

The Kumasi Metropolitan area is approximate 254 km2 and is located between latitudes

6°35” and 6°4”N and longitudes 1°30” and 1°35” E (Ghana Districts, 2006). It shares boundaries with the Kwabre District to the north, Atwima Kwanwoma and Atwima

Nwabiagya District to the west, Ejisu-Juaben Municipal to the east and Bosomtwe District to the south. The metropolis has a human population of 2,035,064 constituting 43% of the total human population of 4,780,380 in the Ashanti region (Ghana Statistical Service, 2012a).

Kumasi is a cosmopolitan city and home to most major ethnic groups from West Africa.

The health services in the municipality are relatively abundant and include the Komfo

Anokye Teaching Hospital (KATH), which is one of the two national autonomous hospitals, four polyclinic which is the urban version of the rural health center, five healthcare centres owned by the Church of Christ and the Seventh-Day Adventist Church, over 200 known private health institutions and 13 industrial clinics (Kumasi Metropolitan Assembly, 2006).

By investigating the use of wild animal based remedies in an urban setting, this study attempts to determine the cultural ties between pangolin use as a source of traditional medicine within a metropolitan area that is relatively well equipped with adequate modern healthcare facilities compared to the more rural areas of Ghana.

4.2.2 Ethics Statement

This study was approved by the ethics committee of the Tshwane University of Technology

(REC Ref #: REC2013/05/008) and written informed consent was obtained from all participants interviewed.

4.2.3 Data collection

Ethnozoological data on medicinal use of pangolins was collected between September 2013 and January 2014 using semi-structured interviews. The sampling process was purposeful with participants intentionally selected because they could provide the relevant information pertinent to this study (Babbie, 2001). Snowball approach, as well as signpost and radio advertisement, was used to identify traditional healers in the metropolis. Of the 62 traditional healers identified to have used or currently using whole or parts of pangolins in their remedies, 48 agreed to participate in this study. Participants were made aware of their rights to decide to either voluntary participate or to decline. The interview questions focused on the interviewees’ knowledge of the uses of pangolin parts or whole pangolins for medicinal purposes to cure or alleviate a particular medical ailment or a set of ailments. Verbal prompts and probes were used to motivate informants and elicit information from them and the pace as well as direction of the interviews was dictated by the participants.

The key questions that were asked to traditional healers (THs) were: (i) do you know the animal called pangolin (participants were shown photographs of African pangolin species) and (ii) do you know whether it is prescribed as a source of medicine? In the semi-structured interviews, the THs (interviewees) were requested to name the parts of pangolins used as

53 medicine, the ailments for which that body part was prescribed and how the animals were obtained. THs were also questioned on how this knowledge was acquired. The interviews were conducted in Twi language which is the most widely spoken language by the Ashanti’s in the metropolis and has also been adopted by many others as a lingua franca. The researcher as well as all the participants interviewed are fluent in the Twi language. Demographic data of traditional healers were also collected.

4.3 Data analysis

Four quantitative value indices were calculated to establish the frequency of use of pangolins or their body parts in TM, as well as the consensus of use body parts among THs: cultural importance index (CI), relative frequency of citation (RFC), informant agreement ratio (IAR), and use agreement value (UAV).

4.3.1 Cultural Importance Index (CI)

Cultural importance index (CI), developed by Tardio and Pardo-de Santayana (2008), takes into account the uniformity of the body part used between THs as well as a body part’s diversity of uses to treat ailments among THs.

푢푁퐶 푖푁 URui 퐶퐼 = ∑ ∑ N 푢=푢1 푖=푖1

where u is the category of use (e.g.: spiritual ailments, rheumatism, infertility), NC is the total number of different categories of use (of each ‘i’ body part), UR is the total number of use-

54 reports for each body part (corresponding in the present study to ‘citations’, as defined above) and N is the total number of informants.

4.3.2 Relative Frequency of Citation (RFC)

This index calculates the frequency of use amongst all the TMPs and is obtained by dividing the number of informants who mention the use of the body part (also known as frequency of citation: FC), by the number of informants participating in the survey (N) (Tardio & Pardo-de

Santayana, 2008). Theoretically, the RFC varies from 0 (when no respondents refer to the body part as useful) to 1 (if all the TMPs made use of a particular body part) (Tardio &

Pardo-de Santayana, 2008). The RFC was calculated using the following formula:

퐹퐶 푅퐹퐶 = 푁

where FC is frequency of citation and N is total number of participants.

4.3.3 Informant Agreement Ratio (IAR)

The Informant Agreement Ratio (IAR) was used to measure the consensus level for treating a particular ailment making use of a particular pangolin body part amongst THs. The original formula proposed by Trotter and Logan (1986) was interpreted as follows:

푛푟 − 푛푎 퐼퐴푅 = 푛푟 − 1

55 where nr is the total number of use reports registered for a body part and na is the number of ailments that are treated with this body part. The IAR value varies between 0 and 1whereby a value of 1 represents the highest level of agreement of a medicinal part.

4.3.4 Use Agreement Value (UAV)

According to Thomas et al. (2009) this index provides a valid and easily derived estimation of the animal’s medicinal cultural significance as a resource. Following the suggestions of

Thomas et al. (2009), but using UV instead of Quality Use Value (QUV), the use agreement value (UAV) was defined as follows:

푈퐴푉 = 퐶퐼 × 퐼퐴푅

where CI is the cultural importance index of body part and IAR is the informant agreement ratio of that body part.

4.4 Results

The majority of participants were between the ages of 51–60 and have practised for more than 20 years (Table 4.1). Regarding gender, the majority were males while Muslims dominated with respect to religion and had a Quranic education. The level of education of the majority of participants was below primary level (Table 4.1). A total of 13 pangolin body parts were identified as being used and prescribed for the treatment of 35 ailments (Table

4.2). Spiritual ailments had the highest use reported (UR) followed (in descending order) by rheumatism, infertility, financial rituals and convulsions (Table 4.2). Pangolin scales had the

56 highest use report (19 of 35 ailments), followed by bones (14 ailments), the head (10) and meat (9), respectively (Table 4.2). The heart and limbs had the lowest UR (1).

Table 4.1: Demographics of participants in the study

Number Percentage Gender Male 45 94 Female 3 6 Age group 31-40 3 6 41-50 8 17 51-60 21 44 60+ 16 33 Number of years of practice 5-10 4 8 11-15 5 10 16-20 8 17 Above 20 31 65 Last level of education Below primary 30 63 Below secondary 13 27 Secondary 4 8 Post-secondary 1 2 Religion Muslim 41 85 Christian 6 13 Animist 1 2

Table 4.2: Use Report (UR) by traditional healers for particular pangolin body parts for the treatment of specific ailments

Body parts Ailments A B C D E F G H I J K L M spiritual protection 6 2 2 1 3 1 1 rheumatism 7 7 1 infertility 1 5 1 1 1 financial rituals 4 1 1 1 1 convulsions 5 1 menstrual pains 3 1 1 stomach disorders 4 1 protection from 1 1 1 2 witchcraft headache 1 1 2 skin scars 4 stroke 1 2 1 waist pain 3 1 heart disease 2 2 back pain 3 asthma 1 2 mental illness 1 1 1 charms for 3 chiefs epilepsy 3 courting a lady 2 bedwetting 1 1 waterborne diseases 2 fever 1 1 gonorrhoea 2 preventing miscarriage 1 1 during pregnancy treating wounds 2 broken leg 1 skin rash 1 body aches 1

Body parts Ailments A B C D E F G H I J K L M scrotal mass 1 prolonged or 1 continuous menstrual bleeding elephantiasis 1 impotence 1 breast cancer 1 leprosy 1 coughing 1 Total 52 24 19 9 5 5 3 3 2 2 2 1 1 A=Scales, B=Bones, C=Head, D=Meat, E=Eyes, F=Tail, G=Whole animal, H=Claws, I=Bile, J=Leg, K=Waist, L=Heart, M=Toes

With regards to the contribution of each of the 13 pangolin body parts to the total cultural importance index (CI), scales had the highest CI followed by the bones, head and meat (Table

4.3). Scales and bones were equally important for the treatment of rheumatism. Scales were also important for spiritual protection and the treatment of convulsions. The head was important for the treatment of infertility while the meat was used for preparing charms for chiefs or tribal leaders. Similar results were obtained when comparing the level of agreement of use of pangolin body parts consistently prescribed by traditional healers for the treatment of particular ailments (i.e. Informant Agreement Ratio, IAR, Table 4.4). Scales had the highest IAR, followed by the head, bones and meat (Table 4.4). Scales were predominantly used to treat rheumatism, followed by spiritual protection, convulsions and financial rituals.

The head was mainly used to treat infertility while the meat was used in the preparation of charms for chiefs.

Table 4.3: Cultural Importance Index (CI) of pangolin body parts and their respective ailments treated

Body parts Ailments A B C D E F G H I J K L M spiritual protection 0.125 0.042 0.042 0.021 0.063 0.021 0.021 rheumatism 0.146 0.146 0.021 infertility 0.021 0.104 0.021 0.021 0.021 financial rituals 0.083 0.021 0.021 0.021 0.021 convulsions 0.104 0.021 menstrual pains 0.063 0.021 0.021 stomach disorders 0.083 0.021 protection from witchcraft 0.021 0.021 0.021 0.042 headache 0.021 0.021 0.042 skin scars 0.083 stroke 0.021 0.042 0.021 waist pain 0.063 0.021 heart disease 0.042 0.042 back pain 0.063 asthma 0.021 0.042 mental illness 0.021 0.021 0.021 charms for chiefs 0.063 epilepsy 0.063 courting a lady 0.042 bedwetting 0.021 0.021

Body parts Ailments A B C D E F G H I J K L M waterborne diseases 0.042 fever 0.021 0.021 gonorrhoea 0.042 preventing miscarriage 0.021 0.021 during pregnancy treating wounds 0.042 broken leg 0.021 skin rash 0.021 body aches 0.021 scrotal mass 0.021 prolonged or continuous 0.021 menstrual bleeding elephantiasis 0.021 impotence 0.021 breast cancer 0.021 leprosy 0.021 coughing 0.021 Total 1.083 0.500 0.396 0.188 0.104 0.104 0.063 0.063 0.042 0.042 0.042 0.021 0.021 A=Scales, B=Bones, C=Head, D=Meat, E=Eyes, F=Tail, G=Whole animal, H=Claws, I=Bile, J=Leg, K=Waist, L=Heart, M=Toes

Table 4.4: Informant Agreement Ratio (IAR) of pangolin body parts and their respective ailments treated

Body parts Ailments A B C D E F G H I J K L M spiritual protection 0.075 0.036 0.053 0.028 0.300 <0.000 <0.000 rheumatism 0.087 0.127 0.050 infertility 0.012 0.132 0.028 0.050 0.167 financial rituals 0.050 0.026 0.028 <0.000 <0.000 convulsions 0.062 0.018 menstrual pains 0.037 0.028 <0.000 stomach disorders 0.050 <0.000 protection from 0.012 0.018 0.050 0.333 witchcraft headache 0.012 0.018 0.053 skin scars 0.050 stroke 0.012 0.036 0.026 waist pain 0.054 <0.000 heart disease 0.025 0.053 back pain 0.037 asthma 0.018 0.053 mental illness 0.012 0.018 0.100 charms for 0.083 chiefs epilepsy 0.037 courting a lady 0.100 bedwetting 0.012 0.018

Body parts Ailments A B C D E F G H I J K L M waterborne diseases 0.025 fever 0.018 0.026 gonorrhoea 0.053 preventing miscarriage 0.028 <0.000 during pregnancy treating wounds 0.025 broken leg 0.018 skin rash 0.018 body aches 0.026 scrotal mass <0.000 prolonged or <0.000 continuous menstrual bleeding elephantiasis <0.000 impotence 0.100 breast cancer 0.018 leprosy 0.012 coughing 0.028 Total 0.647 0.435 0.500 0.250 0.500 0.250 0.000 0.500 <0.000 <0.000 <0.000 <0.000 <0.000 A=Scales, B=Bones, C=Head, D=Meat, E=Eyes, F=Tail, G=Whole animal, H=Claws, I=Bile, J=Leg, K=Waist, L=Heart, M=Toes

Appreciable differences were observed when comparing the various indices with one another

(Table 4.5). With the exception of scales which ranked in first position for all four indices, the order varied for the other body parts depending on the index chosen. The CI, RFC and

UAV indices place bones and the head in second and third positions, respectively. This was not the same for IAR, which ranked the head above the bones. The heart and limbs were the lowest in all indices.

Table 4.5: Evaluation of pangolin body parts using Cultural Importance Index (CI), Relative

Frequency of Citation (RFC), Informant Agreement Ratio (IAR) and Use Agreement Value

(UAV)

Basic Value Indices Ranking Body part UR FC NU CI RFC IAR UAV CI RFC IAR UAV scales 52 29 19 1.083 0.604 0.647 0.701 1 1 1 1 bones 24 15 14 0.500 0.313 0.435 0.217 2 2 3 2 head 19 14 10 0.396 0.292 0.500 0.198 3 3 2 3 meat 9 9 7 0.188 0.188 0.250 0.047 4 4 4 5 eye 5 5 3 0.104 0.104 0.500 0.052 5 5 2 4 tail 5 5 4 0.104 0.104 0.250 0.026 5 5 4 7 whole animal 3 2 3 0.063 0.042 <0.000 <0.000 6 7 5 8 claws 3 3 2 0.063 0.063 0.500 0.031 6 6 2 6 bile 2 1 2 0.042 0.021 <0.000 <0.000 7 8 5 8 leg 2 1 2 0.042 0.021 <0.000 <0.000 7 8 5 8 waist 2 1 2 0.042 0.021 <0.000 <0.000 7 8 5 8 heart 1 1 1 0.021 0.021 <0.000 <0.000 8 8 5 8 toes 1 1 1 0.021 0.021 <0.000 <0.000 8 8 5 8 UR=use report, FC=frequency of citation, NU=number of uses

4.5 Discussion

4.5.1 Cultural importance index (CI)

Pangolin scales are highly valued in African traditional medicine pharmacopoeia where they are widely used. This study confirmed this in that knowledge about pangolin scales used for medicinal purposes was found to be more widespread than any other pangolin body part.

These findings agree with previous studies in Africa in that scales are the most versatile pangolin body part for the treatment of a variety of ailments (Bräutigam et al., 1994; Soewu

& Ayodele, 2009; Soewu & Adekanola, 2011; Chapter 3). Indeed, the suite of ailments treated by pangolin scales in this study was similar to the ailments treated in other African countries (Bräutigam et al., 1994; Akpona, Djagoun & Sinsin, 2008; Soewu & Ayodele,

2009; Soewu & Adekanola, 2011; Chapter 3). Not only were scales prescribed for physical medical ailments but they were also prescribed to prevent or inhibit spiritual ailments as was found to be the case in previous studies (Akpona, Djagoun & Sinsin, 2008; Soewu &

Ayodele, 2009; Soewu & Adekanola, 2011; Chapter 3).

The relatively high CI index for pangolin bones also suggests that bones have an important role to play in traditional healing practices and previous studies have also indicated that they are prescribed for the treatment of rheumatism, stroke and pains in Nigeria (Soewu &

Ayodele, 2009; Soewu & Adekanola, 2011) and Sierra Leone (Chapter 3). This study, however, found the versatility of pangolin bones for the treatment of more than one ailment to be greater in Ghana than was indicated for Nigeria (Soewu & Ayodele, 2009; Soewu &

Adekanola, 2011) and Sierra Leone (Chapter 3). Pangolin heads have previously been recorded being used to treat fever in Benin Republic in West Africa (Akpona, Djagoun &

Sinsin, 2008) and for treating spiritual ailments in Nigeria (Soewu & Ayodele, 2009; Soewu

& Adekanola, 2011). This study also found the head to be very important in the treatment of infertility, headache and heart diseases which has also been found to be the case in Sierra

Leone (Chapter 3).

Bräutigam et al. (1994) found pangolin meat to be less valued for medicinal purposes compared to other body parts, however this study indicates that among the 13 pangolin body parts used by traditional healers, the meat was the fourth most culturally important after scales, the head and bones. However, knowledge about the therapeutic abilities of the meat was less widespread and was mostly limited to the preparation of charms for chiefs. The eyes were primarily prescribed for spiritual protection but were also used to treat kleptomania as was found in Nigeria (Soewu & Ayodele, 2009; Soewu & Adekanola, 2011) and Apollo

(acute haemorrhagic conjunctivitis) in Sierra Leone (Chapter 3). The pangolin heart had a very low index value and was occasionally used to prevent miscarriage in Ghana although

Akpona, Djagoun and Sinsin (2008) documented the use of pangolin heart and leg to treat tachycardia, and promote normal growth and vigour in babies in Benin Republic. The low use value and medicinal application of the bile, leg, heart, waist, claws and toes are indications that these pangolin body parts are culturally less important to the traditional healers of Ghana than other body parts.

4.5.2 Informant Agreement Ratio (IAR)

The high IAR for scales and bones is an indication that these items are important components of local cultural knowledge within the traditional healer community (Heinrich et al., 2009) and an indication that a particular pangolin part is preferred in the community for treatment

66 of specific ailments (Gazzaneo, Lucena & Albuquerque, 2005; Almeida et al., 2006; Alves &

Rosa, 2006). On the contrary, the low IAR for the whole animal, bile, leg, waist, heart and toes may be an indication that these body parts have either fallen into disuse because of cultural adaptation or are believed to be ineffective for treating conditions or ailments or may simply be of a low cultural importance in traditional medicine. Culturally bound syndromes are usually bound to yield high consensus values due to their folk nature (Heinrich et al.,

1998) with traditional healers often preferring a particular body part for the treatment of a particular ailment because belief systems do not usually permit the prescription of a substitute resource as a form of medical treatment. This study found culturally bound syndromes such as spiritual ailments, financial rituals, protection from witchcraft, preparation of charms for chiefs as well as courting ladies scoring high IAR for particular body parts used. For instance, there may not be any other substitute part for the pangolin meat which was the only body part used in the preparation of charms for chiefs.

One disease that was surprisingly not mentioned but that is widespread in the study area and impacts upon a large number of local communities is malaria. The selection and use of a resource for traditional medicinal purposes are usually based on culturally perceived effectiveness (Heinrich et al., 1998) that is generally handed down from generation to generation. The perceived ineffectiveness of pangolin body parts for the treatment of malaria may have accounted for its noticeable absence in the list of diseases mentioned by traditional healers.

4.5.3 Comparing different indices

With the exception of scales, which occupied the top ranking for all indices, the other body parts varied in their ranking in the different indices. The distribution of knowledge about traditional remedies follows a pattern whereby few remedies are known to almost everyone while most knowledge is idiosyncratic (Thomas et al., 2009) and this idiosyncrasy may account for the variation in indices for body parts, particularly for the IAR.

Training to become a traditional medical practitioner within Ghana is either via family tradition or an informal apprenticeship (Twumasi, 1979; Abel & Busia, 2005). Trainees undergo a period of training during which he/she learns the curative potential of plants, animals and minerals through the observation of their “master healer” (Twumasi, 1979;

Omolewa, 2007). Those traditional healers that partook in this study were all trained via a family tradition and obtained their knowledge verbally from either a mother, father, uncle or grandparent and therefore this knowledge is likely to be idiosyncratic in nature and, in turn, would influence the results and the consensus on use of a particular pangolin body part.

Thomas et al. (2009) established that the combination of the number of use reports and the level of consensus between participants seems to provide a valid and easily derived estimate of cultural significance and it can therefore be deduced that the culturally important pangolin body parts found in this study, such as scales, bones and head, are those with high use agreement values. It is therefore proposed that pangolins have been utilised for some time as a constant and frequent source of traditional medicine and it plays a large culturally important role in Ghanaian traditional pharmacopoeia.

4.6 Conservation implications

All three species of African pangolin that occur within Ghana; the white-bellied pangolin

(Phataginus tricuspis), black-bellied pangolin (Phataginus tetradactyla) and the giant ground pangolin (Smutsia gigantea) have been up-listed to Vulnerable on the recently revised IUCN

Red List (Challender, Waterman & Baillie, 2014). In addition, the Wildlife Conservation Act

1971 (LI 685) classifies them as Schedule 1 and this prohibits their hunting or possession.

Despite their conservation and protection status, pangolins are still being hunted for their purported medicinal values and the law regarding the protection of the species is not enforced. Based on the CI, IAR and UAV indices, where pangolin body parts are used to treat ailments by traditional healers, this study has found that the use of pangolins in local community pharmacopoeia is quite common. However, if this use and harvest is unsustainable and off-take exceeds recruitment into the population, it can have drastic consequences on their natural population status (Alves & Rosa, 2005; Alves & Santana,

2008; Alves et al., 2008). With such apparent frequent use, it is of concern that the harvest of these endangered mammals is unsustainable, particularly when most of the trade in pangolins is informal.

Furthermore, these results indicate that pangolins are used to treat folk illnesses which usually have no substitute or alternative remedies with healers relying on what they are culturally familiar with. This use of pangolins to treat folk illnesses, such as protection against witchcraft, spiritual protection and the courting of ladies, can be considered an additional threat to the level of harvesting of pangolins in Ghana as these illnesses are considered to be intrinsic to the Ghanaian cultural concepts of health and illness (Twumasi,

1979; de-Graft Aikins et al., 2012). The rate of harvest is further increased by the high CI of

69 pangolin body parts for ailments that have been found to be medically or socially prevalent in

Ghana. Rheumatism, which has a high CI, has been listed among the top 10 diseases seen at outpatient departments in hospitals and clinics across Ghana (Ghana Health Service, 2010), and convulsions are also common due to Ghana being a malaria hyper-endemic country

(Department for International Development (DFID), 2011) President’s Malaria Initiative,

2012). Again, infertility has a high CI index for pangolin body parts and is considered a social problem in the country and the belief in superstitions is most often ‘cured’ or remedied via traditional healers prescribing pangolin body parts (Tabong & Adongo, 2013). The fact that most of the body parts used by traditional healers can only be obtained after killing the animal raises further concerns about the impact that harvesting pressure has on pangolins.

Furthermore, there are no ex situ breeding facilities for African pangolins, thus all individuals that are used for medicinal purposes are being obtained from the wild (Soewu & Ayodele,

2009; Soewu & Adekanola, 2011). Even though the healing properties and effectiveness of pangolin body parts have not been scientifically tested, they remain of large cultural significance due to their purported healing properties and the harvest of these species will continue unabated. These cultural medical knowledge systems are often organised within local cultural communities (Costa-Neto, 2004) and the belief system of TMPs may not offer a substitute for a particular remedy thus making sole reliance on pangolin body parts inevitable.

A tribe or community’s cultural and traditional background and belief systems rather than pharmacological properties often plays a greater role in determining the effectiveness of traditional medicine (Moerman, 2007).

The impact that traditional medicine is having on the survival and conservation status of wild pangolin populations should be considered as an important population threat to these

70 mammals just as other anthropogenic pressures may be (Challender & Hywood, 2012;

Pietersen, McKechnie & Jansen, 2014a). This form of harvest on wild pangolin populations should be carefully assessed and monitored as current turn-over rates in the utilisation of these species for traditional medicine is not known and very little data exists on current population levels and distribution of these three species in Ghana (Challender et al., 2014).

Furthermore, little information exists on the levels of trade and harvest of biodiversity from the wild that is used for traditional medicine in Ghana (Ministry of Health, 2005). It is therefore important that conservationists increase their understanding of the biology, ecology and population status of species commonly used as traditional remedies to better assess the impact of harvesting on wild populations (Alves, Rosa & Santana, 2007). As such, conservation strategies for pangolins in Ghana would first need to focus on understanding the current population status, biology and ecology of the species in order to effectively assess the effect of this harvest on wild populations. In the meantime, conservation efforts should be aimed at educating traditional healers on the implications of unsustainable harvest of wild pangolins and the potential threat that the loss of these species may have on local community cultural belief systems if they are no longer available.

4.7 Conclusion

The cultural belief system is most likely to be the driving force for the maintenance and continued use of pangolins in urban environments for medicinal purposes. Popular knowledge about the curative properties of pangolin body parts is an integral part of the local culture and demonstrates the necessity of carefully studying the use of pangolins for therapeutic practices to better understand the human cultural interaction. There is a need to undertake multidisciplinary studies to investigate the social, cultural, and economic aspects of

71 pangolin use in traditional medicinal practices in Africa in order to develop sound conservation management strategies and action plans for these species.

CHAPTER 5

UNRAVELLING THE PANGOLIN BUSHMEAT COMMODITY CHAIN AND THE EXTENT OF TRADE IN GHANA

5.1 Introduction

Mammals are regarded as the prime source of bushmeat throughout Africa (Ntiamoa-Baidu,

1987; Fa et al., 2006; Fa & Brown 2009; Schulte-Herbrüggen et al., 2013a). One such group of mammals that has long been hunted throughout their range in Africa and consumed for bushmeat are pangolins (Anadu, Elamah & Oates, 1988; Bräutigam et al., 1994; Sodeinde &

Adedipe, 1994; Njiforti, 1996; Caspary, 1999; Fa & Gracía Yuste, 2001; Conservation

International-Ghana 2002; Fa et al., 2002; Fa et al., 2006; Crookes et al., 2007; Bokhorst,

2010; Foerster et al., 2012; Schulte-Herbrüggen et al., 2013a; African Pangolin Working

Group, 2014; Soewu & Sodeinde 2015). Evidence suggests that the current off-take levels of mammals for bushmeat purposes are unsustainable (Milner-Gulland & Akçakaya 2001;

Milner-Gulland et al., 2003; Fa & Brown 2009). Various methods have been used to determine the sustainability of harvest with market indices being the most widely used indicator in Africa (Weinbaum et al., 2013). Major bushmeat market surveys have been used with relative success to determine the level of hunting pressure in Ghana (Ntiamoa-Baidu,

1987; Rowcliffe, Cowlishaw & Long, 2003; Crookes, Ankudey & Milner-Gulland, 2005;

Cowlishaw, Mendelson & Rowcliffe, 2005a).

While pangolins were identified among the 11 most preferred wild animal species in a survey to determine the bushmeat preferences among Ghanaians (Conservation International-Ghana

2002), extensive bushmeat market surveys by researchers have failed to record the actual

73 extent of pangolins traded or the turnover rates over time (Ntiamoa-Baidu, 1987; Hofmann,

Ellenberg & Roth, 1999; Cowlishaw, Mendelson & Rowcliffe, 2005a, b). Thus far only

Crookes, Ankudey and Milner-Gulland (2005) recorded one individual pangolin in a survey of a single large bushmeat market in Ghana between January 1987 and July 2002.

Conservation International-Ghana (2002) recorded two individual pangolins in their survey of

16 major bushmeat markets in Ghana. The disparity between the lack of recordings of pangolin in bushmeat markets and the high preference for pangolin bushmeat may indicate that pangolins do not follow a typical pattern for bushmeat market in Ghana. The use of market surveys is based on the assumption that all species of concern make it to major bushmeat markets (Allebone-Webb et al., 2011; Kamins et al., 2011; Weinbaum et al., 2013).

However, factors including sales at village level, distance to major bushmeat markets, level of law enforcement influence the volume in these markets and should also be taken in to account (Fa et al., 1995; Fa et al., 2006; Crookes et al., 2007; Weinbaum et al., 2013) As such, the existing bushmeat market surveys may therefore be underestimating the impact of bushmeat harvest on the natural population of pangolins in Ghana.

Although the characteristics of the bushmeat commodity chain have been investigated in

Ghana (Mendelson, Cowlishaw & Rowcliffe, 2003; Cowlishaw, Mendelson & Rowcliffe,

2004; Cowlishaw, Mendelson & Rowcliffe, 2005a, b; Bokhorst, 2010), no attempt has been made to establish the number of pangolin species traded outside of major markets. As all four species of Africa’s pangolins are listed as Vulnerable by the IUCN (2014), the primary aim of this study was to evaluate the number and species composition of threatened pangolins that are traded along the bushmeat commodity chain in Ghana with regards to various role players and distances from protected areas.

5.2 Materials and methods

5.2.1 Study area

We conducted a reconnaissance survey to determine where pangolins are traded for bushmeat purposes outside of major bushmeat markets in Ghana. Based on the reconnaissance survey,

10 study sites spanning five out of 10 political administrative regions in Ghana were chosen based on recorded sightings of pangolin for bushmeat sales. Konogo (A), New Edubiasi (B),

Wiaso (C) and Tepa (D) (Ashanti region), Goaso (E) (Brong-Ahafo region), Dunkwa-on-

Offin (F) and Assin Fosu (G) (Central region), Anyinam (H) (Eastern region) and Wassa

Akropong (I) and Wassa Nkonya (J) (Western region) were the towns (sites) chosen for this study (Figure 5.1).

Figure 5.1: Map of Africa indicating Ghana’s administrative regions and the study sites

Within these areas, data was collected from all known markets or bushmeat selling points. Of the study sites chosen, Conservation International-Ghana (2002) identified Konogo, Tepa,

New Edubiasi and Goaso, while Osei-Tutu et al. (2012) identified Anyinam as major sources of supply of bushmeat. All the study sites fell under the High Forest Zone of Ghana, which is situated in the Upper Guinea Forest global biodiversity hotspot and this region is considered to have a high diversity of flora and fauna (Myers et al., 2000). Farming is the primary economic activity within these regions, with cocoa and maize being the two most important cash crops and accounting for 95% of the total harvest value of crops (Ghana Statistical

Service, 2008). Conversion of land cover for cocoa farming as well as bushmeat hunting are some of the major threats contributing to a reduction in biodiversity in this ecological zone

(Ministry of Environment and Science-Ghana 2002).

5.2.2 Ethics statement

This study was approved by the ethics committee of the Tshwane University of Technology

(REC Ref #: REC2013/05/008) and written informed consent was obtained from all participants interviewed. All data were anonymised to reduce the risk of harm to informants.

5.2.3 Data collection

Data collection was conducted between September 2013 and January 2014 in order to cover both wet and dry seasons. This period has been described as statistically adequate by Fa et al.

(2006) based on Fa et al.’s (2004) assessment of the efficiency of various methods for measuring the volume of bushmeat extracted and proportion of species traded in west and central African studies. Data collection focused on farmer hunters (who act as the primary

76 source of bushmeat for the other stakeholders and hunt part-time to supplement their income especially during lean farming periods), wholesalers (who usually operate from their home and buy bushmeat in bulk from the farmer hunters and sell to the retailers), and chopbar operators (who are by far the most numerous group in the chain and operate cafés specialising in traditional meat stews containing bushmeat, domestic meat or fish with a substantial number of clientele) (Mendelson, Cowlishaw & Rowcliffe, 2003; Cowlishaw,

Mendelson & Rowcliffe, 2004; Cowlishaw, Mendelson & Rowcliffe, 2005a, b). Commercial hunters were excluded due to the lack of people solely dependent on hunting for their livelihood in Ghana in recent years (Kamins et al., 2011; Schulte-Herbrüggen et al., 2013a) as well as large urban bushmeat market surveys since they have failed to record pangolins

(Ntiamoa-Baidu, 1987; Hofmann, Ellenberg & Roth, 1999; Cowlishaw, Mendelson &

Rowcliffe, 2005a, b) or have recorded very few pangolins (Conservation International-

Ghana, 2002; Crookes, Ankudey & Milner-Gulland, 2005). Although the bushmeat commodity chain differentiated between wholesale traders and market traders (who are supposed to operate from stalls in the market), this study did not see much difference between their operations at local level since they both operated from their homes and therefore referred to both as wholesalers in this study. Bokhorst (2010) also found market traders in rural areas to act more or less in their roles as wholesalers in Ghana.

Purposeful sampling approach, which involves the selection of participants more knowledgeable on the study subject, and a snowball sampling approach, which is the use of a targeted population to recommend other members of that population (Babbie 2004) were used. These approaches ensured that participants who could provide information pertinent to this study were selected as representatives of the bushmeat commodity chain.

Data was collected from each stakeholder through a combination of direct observation and semi-structured interviews (as suggested by Cowlishaw, Mendelson & Rowcliffe, 2005a, b).

A total of 153 stakeholders comprising 84 chopbar operators, 48 farmer hunters and 21 wholesalers were interviewed. In the majority of small rural communities in Ghana, buyers and sellers converge on a given location and day to buy and sell goods on a periodic basis; commonly referred to as ‘market day’. In southern Ghana, a seven-day market cycle is the common period for many of the markets (Fagerlund & Smith, 1970). Thus a seven-day market cycle was chosen for this study since most hunters usually target market days to sell their produce and may likely recall accurately the number of a particular species that they have killed or traded within a week. Hence, the interview questions focused on the number of pangolins traded by individual stakeholders within a seven-day cycle. Verbal prompts and probes were used to motivate informants and elicit information from them and the pace as well as direction of the interviews was dictated by the participants. The key questions that were posed to actor groups dealt with: (i) number of pangolins traded, (ii) the hunting technique used for capture, (iii) variation in price and (iv) availability of storage facilities for trade. Distance from protected forest was also estimated due to the high level of poaching in protected forested reserves in Ghana (Jachmann 2008). Direct observations were used to verify information provided by the stakeholders through seven-day market cycle visitations.

5.2.4 Statistical analyses

All statistical analyses were completed with the statistical software package STATISTICA 12

(StatSoft Inc. 2013). The observed and expected pangolins traded among stakeholders were tested using a chi-square test (χ²). To determine whether distance from protected forest affected pangolin number traded, a simple linear regressions and Pearson’s correlation

78 coefficient (r) were used as a measure of the strength of association between the two variables.

5.3 Results

A total of 341 pangolins were recorded to have been traded by farmer hunters, chopbar operators and wholesalers between September 2013 and January 2014. Of this number, 98 individual pangolins were physically observed (83 carcases and 15 live individuals) of which

42 were female and 38 were male white-bellied pangolins (Phataginus tricuspis), and 10 were female and 8 male black-bellied pangolins (Phataginus tetradactyla) (Table 5.1). The mean number of pangolins traded by each stakeholder indicates that wholesalers being the least numerous had the largest per capita market share (Table 5.1).

Table 5.1: Number of pangolin species physically observed to be traded by stakeholders

Stakeholder group Phataginus Phataginus Total number Per capita

tricuspis tetradactyla of pangolins share of

observed stakeholders

Farmer hunters 17 3 20 0.42

Chopbar operators 33 5 38 0.45

Wholesalers 30 10 40 1.90

80 18 98 0.64

Turnover rates were very high with significantly fewer pangolins being encountered than expected within the study period for farmer hunters (χ² = 107.25, df = 4, P < 0.01), chopbar operators (χ² = 48.02, df = 4, P < 0.01) and wholesalers (χ² = 25.70, df = 4, P < 0.01). Most of the wholesalers had a storage facility in the form of (fridge or freezer) purposefully for

79 storage of bushmeat while chopbar operators also had storage facilities but this was largely multipurpose.

The primary route of trade for pangolin bushmeat is from farmer hunters to chopbar operators and wholesalers (Figure 5.2). There was also a flow in trade from wholesalers to local chopbar operators, consumers and city wholesalers.

Figure 5.2: Trade flow patterns in the pangolin bushmeat commodity chain

A significant difference was observed between months based on the number of pangolins traded by stakeholders (KW = 49.540, P < 0.01) (Figure 5.3). Dunn's multiple comparisons test revealed a significantly lower trade in December 2013 over the other months with the exception of November 2013, and trade levels in November 2013 were also significantly lower than in September 2013.

Figure 5.3: Total number of pangolins traded for all study sites by all stakeholders in each study month

With the exception of December 2013, a significant difference was observed amongst all stakeholders (KW = 1.84, P < 0.39) for the number of pangolins traded (Figure 5.4). In the month of September (KW = 12.52, P < 0.01) and October (KW = 14.98, P < 0.01), Dunn's multiple comparisons test revealed a significant difference between chopbar operators and hunters as well as chopbar operators and wholesalers but no significant difference between hunters and wholesalers. Dunn's multiple comparisons test among stakeholder groups revealed a significant difference between wholesalers and chopbar operators as well as wholesalers and hunters but no significant difference between hunters and chopbar operators in November (KW = 18.75, P < 0.01) while the only significance among stakeholders for the month of January 2014 (KW = 11.38, P < 0.01) was between chopbar operators and hunters

(Figure 5.4).

Figure 5.4: Mean number of pangolins traded by stakeholder groups in each study month

The distance from protected forest areas from which pangolins are sourced had a pronounced impact on the number of pangolins being traded in that increased distance from these protected areas reduced the number of pangolins being traded significantly for farmer hunters

(r = -0.77, P < 0.01), chopbar operators (r = -0.61, P < 0.01) and wholesalers (r = -0.71, P <

0.01) (Figure 5.5).

Figure 5.5: The negative relationship between the distance from where pangolins are sourced in protected areas and the number traded in all sites by all stakeholders

Farmer hunters obtained their lowest price from wholesalers across all study sites (Ghanaian

Cedi (GHC) 20, US$ = 9; where US$1 = GHC2.2 at the time of the study) and chopbar operators (GHC30, US$14), and direct sales to consumers, often located on busy roadside verges, were between GHC40 and 50 (US$18-23). Live pangolins fetched a substantially higher price of between GHC80 and 100 (US$36-45) being the highest selling price recorded at Anyinam, however the average prices did not vary much across all study sites. Wholesalers were found to be more selective in their trade with farmer hunters, rejecting badly wounded pangolins or those that had been in snares for long periods; the direct opposite applied for chopbar operators.

With regard to current hunting techniques, wire snares and shotguns were the two widely used methods. 90% (n=75) and 10% (n=8) of the observed carcases were killed using wire snares and shotguns, respectively. None of the respondents were aware of the current conservation status of African pangolins, but they were aware of laws prohibiting the hunting of game animals, including pangolin, within the closed hunting season covering the period 1st

August to 1st December which fell within this study time.

5.4 Discussion

This study’s estimates of numbers of pangolins traded in the bushmeat commodity chain suggest that pangolin harvests have been severely under-reported in previous studies. The pangolin bushmeat commodity chain, which is primarily not geared towards the major bushmeat markets, may explain the under-reporting of pangolin harvesting for bushmeat purposes in Ghana. This finding is corroborated by Kamins et al. (2011), who found under- reporting of the African straw-coloured fruit bat (Eidolon helvum) in major bushmeat market surveys in Ghana because most of their trade occurred completely outside the formal market.

This study found chopbar operators to be the dominant retailers in the pangolin bushmeat trade, accounting for the majority of sales to the public. This finding corroborates studies by

Caspary (1999) and Bokhorst (2010), who also found chopbar operators to be the main intermediaries for the sale of bushmeat in rural areas of Côte d’Ivoire and Ghana, respectively. Mendelson, Cowlishaw and Rowcliffe (2003) and Cowlishaw, Mendelson and

Rowcliffe (2005a) also found chopbar operators to account for the majority of bushmeat sales to the public in urban markets in Ghana. These findings may therefore suggest that the majority of pangolin trade is not within but outside of major bushmeat markets in Ghana

(Ntiamoa-Baidu, 1987; Hofmann, Ellenberg & Roth, 1999; Cowlishaw, Mendelson &

Rowcliffe, 2005a, b).

This study’s per capita market share of wholesalers was consistent with other studies

(Mendelson, Cowlishaw & Rowcliffe, 2003; Cowlishaw, Mendelson & Rowcliffe, 2004;

Cowlishaw, Mendelson & Rowcliffe, 2005a; Bokhorst 2010) which also found wholesalers to have the largest per capita market share of the bushmeat trade due to their small number and position in the commodity chain. Cowlishaw, Mendelson and Rowcliffe (2005a) found that storage facilities, such as fridges, limit the volume and sales of stakeholders in the bushmeat commodity chain. However, this study found that the majority of wholesalers owned a storage facility (fridge or freezer). This may increase their willingness to buy from sellers and therefore increase the per capita market share. Mendelson, Cowlishaw and Rowcliffe (2003) found a more rapid turnover for bushmeat among stakeholders in the bushmeat commodity chain due to a lack of storage facilities. The storage capabilities of wholesalers may account for their relatively high number of pangolins in their possession compared to other stakeholders, since they were not under duress to sell meat before it spoils due to lack of storage capabilities. With regard to market price, these results are similar to those of

Mendelson, Cowlishaw and Rowcliffe (2003), who found that prices offered to hunters by chopbar operators were higher than those offered by wholesalers as well as prices for live animals being sold for twice the amount for the same species.

Evidence of increased hunting during lean farming periods has been observed in Ghana

(Hofmann, Ellenberg & Roth, 1999; Mendelson, Cowlishaw & Rowcliffe, 2003; Crookes et al., 2007; Jachmann, 2008; Brashares et al., 2011; Schulte-Herbrüggen et al., 2013a).

September and October are considered the non-peak season for cocoa production, being the

85 main economic activity in the study sites requiring minimum labour input, while November and particularly December are considered peak seasons requiring high labour (Mull &

Kirkhorn, 2005; Schulte-Herbrüggen et al., 2013b). It seems likely that the high number of pangolins traded in September and October was due to the low labour demands on cocoa farms, thus increasing hunting activities. Caspary (1999) observed a similar trend in that hunting activities increase during the non-peak cocoa months of September and October in the forest regions of Côte d’Ivoire. Similar pangolin trade numbers were found in Equatorial

Guinea (Fa & Gracía Yuste, 2001) although no explanations for the observed fluctuations were given. Variation in labour demand may also have been a possible cause.

While the potential value of the agricultural landscape or farmbush matrix to indigenous wildlife has been well documented (Cowlishaw, Mendelson & Rowcliffe, 2005a, b; Crookes et al., 2007; Schroth & Harvey, 2007; Cassano et al., 2008; Newmark, 2008; Schroth et al.,

2011), wildlife is disappearing from unprotected lands in Africa. Hunters are therefore increasingly focusing their efforts on the nearest protected areas simply based on the availability of more prey (Lindsey et al., 2013). This study found that stakeholders closer to protected areas traded more pangolins compared to those distant from protected forests.

These findings were consistent with those of Fa et al. (2006), who also found that the numbers of animals traded declined dramatically further away from the Korup (Cameroon) and Cross River (Nigeria) National Parks. Similar results have been observed in Côte d’Ivoire

(Caspary, 1999), Equatorial Guinea (Fa & Gracía Yuste, 2001; Fa, Ryan & Bell, 2005),

Gabon (Foerster et al., 2012) and in Ghana (Schulte-Herbrüggen et al., 2013b). This hunting in close proximity to protected areas essentially equates to decreased time, effort and costs for hunters to find wildlife (Hofer et al., 2000). Therefore farmer hunters are more likely to focus their off-take efforts on nearby protected areas.

5.5 Conservation implications

All three species of African pangolin that occur within Ghana, i.e. the white-bellied pangolin

(Phataginus tricuspis), black-bellied pangolin (Phataginus tetradactyla) and the giant ground pangolin (Smutsia gigantea), have been listed as Vulnerable on the recently revised IUCN

Red List (IUCN, 2014) and are listed on CITES Appendix II. In addition, the Wildlife

Conservation Act of 1971 (LI 685) classifies pangolins under Schedule 1, prohibiting any person from hunting or being in possession of pangolins. This makes all trade in pangolins in

Ghana illegal due to the ban on hunting that was in place within the months of 1st August to

1st December when data collection was on-going. Clearly, the high volume of pangolins encountered is an indication that wildlife laws are not serving as a deterrent to the poaching of pangolins for bushmeat purposes in Ghana or it is simply not being enforced.

The use of snares is illegal for hunting practice in Ghana (Conservation International-Ghana

2002) and the disregard for or poor enforcement of conservation laws in Ghana may also be the reason behind the use of snares for hunting pangolins. According to Fa, Ryan and Bell

(2005), any wildlife management programme in African forests must address the issue of snares as a hunting technique. Snares are non-selective with regard to species, age and sex

(Noss, 1998; Fa & Gracía Yuste, 2001; Willcox & Nambu, 2007) and their ease of access as well as affordability in Ghana (Crookes et al., 2007) will allow hunters to reduce replacement costs of snares and operate in more extensive areas. This may, in turn, have implications for pangolin survival and reproduction. Furthermore, economic and cultural drivers as well as weak enforcement of conservation laws may increase hunting pressure, particularly within protected areas. This will have severe consequences on biodiversity since it will influence the viability of endangered species in protected refuges (Fa et al., 2006).

Species, such as pangolins, with slow reproductive rates are at a higher risk of extinction

(Johnson, 2002). Such species are more susceptible to extinction by hunting because they are less resilient to increased mortality from hunting (Price & Gittleman, 2007). This theory is critical to the susceptibility of pangolins since they are known to have very slow reproductive rates at one pup per female per year (Kingdon 1971; Sodeinde & Adedipe 1994; Gaubert,

2011). High levels of hunting may threaten their survival since they are already under threat from habitat destruction and being killed for medicinal uses. Furthermore, there is little knowledge about their fundamental and basic biological and ecological characteristics and this knowledge is needed in order to make informed decisions with regards to the sustainability of harvesting pangolins (Fa & Brown 2009). However, reproductive seasonality, maturation, fecundity, feeding ecology, abundance, distribution and ecology of pangolins in African forests are still poorly known (Gaubert, 2011; Challender et al., 2014).

This information is also needed in order to improve ability to evaluate the impact of hunting in addition to market demand indices and hunting levels to propose suitable pangolin conservation management actions.

5.6 Conclusion

This study reveals that the pangolin bushmeat trade was previously underestimated in Ghana.

This can be due to the lack of monitoring within the bushmeat community chain that results in the underestimation of their harvest levels. Considering the current extent of hunting and trading in pangolins, the bushmeat trade should be monitored more effectively and regularly to predict off-take levels. Furthermore, effective laws are currently in place for African pangolins in Ghana but there is evidence to suggest that they are not being implemented. As an alternative, the use of media platforms to educate and create awareness within the general

88 public with regards to the conservation status of African pangolins may provide a mechanism to reduce the harvest of this group of endangered mammals and to utilise them more sustainably.

CHAPTER 6

LOCAL ECOLOGICAL KNOWLEDGE OF PANGOLINS AMONG HUNTERS IN

GHANA AND SIERRA LEONE

6.1 Introduction

Pangolins are mammals that are widely harvested for busmeat purposes and for their purported medicinal value in sub-Sahara Africa (Fa et al., 2006; Akpona, Djagoun & Sinsin,

2008; Gaubert, 2011; Soewu & Adekanola, 2011; Foerster et al., 2012; Kingdon & Hoffman,

2013; Setlalekgomo, 2014; Chapters 3 and 4). This prevalent utilization of pangolins together with other factors, such as habitat loss, can contribute to severe population declines of an already highly threatened group of animals and could likely lead to their local extirpation.

Currently all four African pangolin species, namely black-bellied pangolin (Phataginus tetradactyla), white-bellied pangolin (P. tricuspis), Temminck’s ground pangolin (Smutsia temminckii) and the giant ground pangolin (S. gigantea) are listed on CITES Appendix II and have been up-listed to vulnerable on the recently revised IUCN Red List (IUCN, 2014).

Pangolins are also susceptible to extinction based on their slow reproductive rates (Kingdon,

1971; Sodeinde & Adedipe, 1994; Gaubert, 2011; Kingdon & Hoffman, 2013). Little is currently known about the biology, ecology and conservation needs of pangolins, particularly the four African pangolin species, in spite of the numerous threats that they face (Gaudin,

Emry & Wible, 2009; Gaubert, 2011; Kingdon & Hoffman, 2013; Challender et al., 2014).

Local ecological knowledge (LEK) is useful for a population assessment study of a particular species in addition to providing biological and ecological information of species where little

90 or no empirical data exist (Ferguson, Williamson & Messier, 1998; Huntington, 2000).

Furthermore, the use of LEK as a potential means for expanding the sources of information for ecosystems and their associated biodiversity is widely acknowledged (Berkes, 1993;

Huntington, 2000; Olsson & Folke, 2001; Huntington et al., 2004; Gilchrist, Mallory &

Merkel, 2005). Indeed, the incorporation of LEK into conservation planning has been shown to yield benefits towards conservation outcomes at both the local and landscape scales (Baird

& Flaherty, 2005; Sheil et al., 2006). Thus, the use of local stakeholders’ knowledge to optimise decisions is recognised within conservation planning disciplines and is seen as an integral part of conservation planning (Margules & Pressey 2000; Pressey & Bottrill, 2009).

Resource gatherers (hunters or collectors) are individuals who generally have considerable

LEK since their success at harvesting is often directly linked to their ecological knowledge of a particular species, their ability to interpret tracks and the general knowledge they have on the behaviour of animals (Alves, Nishida & Hernandez, 2005; Alves et al., 2009; Gilchrist,

Mallory & Merkel, 2005). Considering that pangolins form an integral part of local cultures and traditions in both Ghana and Sierra Leone, and that these animals are being hunted extensively within these local communities (Chapters 3 and 4), there possibly exists a large and important LEK regarding pangolins. This knowledge could contribute significantly towards a better understanding of these threatened mammals’ population distribution, ecology and biology of which very little known. The aims of this study were to determine the level of LEK relating to pangolins with respect to morphology, ecology, biology and conservation and how it can be integrated with scientific ecological knowledge for use in planning conservation activities for pangolins in the forests of West Africa.

6.2 Methods

6.2.1 Study area

The study sites fell within the Upper Guinea Forest, a global biodiversity hotspot in Ghana and Sierra Leone that is considered to have a high diversity of flora and fauna (Myers et al.,

2000; Kouame et al., 2012). The loss of forest habitat is primarily due to fragmentation through conversion to agriculture, increased human settlement as a result of the rapid population growth and expansion in these countries, large-scale bushmeat hunting and mining activities (Kouame et al., 2012). Eight study sites were chosen based on reported sightings of pangolins for sale by means of a reconnaissance survey due to the lack of data on the population size and distribution of pangolins in both countries. The Ashanti, Brong-Ahafo,

Central, Eastern and Western regions were chosen in Ghana while the districts of Bombali,

Kenema and Kailahun were chosen in Sierra Leone (Figure 6.1). Farmer hunters within the vicinity of the towns of Konogo, New Edubiasi, Wiaso, Nyinahin and Tepa (Ashanti region),

Goaso and Mim (Brong-Ahafo region), Dunkwa-on-Offin and Assin Fosu (Central region),

Anyinam and Nkawkaw (Eastern region), Wassa Akropong and Wassa Nkonya (Western region) were chosen for this study in Ghana. Makari, Magbingbi, Binkolo, Mato, Moi,

Kamabai and Masama (Bombali district), Lelahun, Jagbwema, Belebu, Saama, Baiama and

Joru (Kenema district), Jojoima, Daru, Njala, Levuma and Manowa (Kailahun district) were the study sites chosen for farmer hunters and palm wine tappers in Sierra Leone. With the exception of Kenema district in Sierra Leone, 46.5% of the population depends on farming as their primary source of income, 89.4% and 60.5% of people living in Kailahun and Bombali districts, respectively, also depends on farming (World Bank, 2013). A similar trend was found in Ghana, where in excess of 40% of the population in the study regions depended on

92 farming as their primary source of income with the exception of the Ashanti region where only 28% of the population are dependent on farming (Ghana Statistical Service, 2012b).

Figure 6.1: Map of the study regions in Ghana and Sierra Leone

6.2.2 Ethics statement

All interviews were conducted with prior consent of the informants. This project was approved by the Research Ethics Committee (number 099/07) of the Tshwane University of

Technology, South Africa.

6.2.3 Data collection

Potential interviewees were identified on the basis of their reputation as hunters of pangolins in their communities and were viewed as the most knowledgeable individuals about the species in question. A purposeful sampling approach was used with participants selected because they could provide the information about issues identified to be important to this study (Creswell, 2003). Farmer hunters (who hunt on a part-time basis to supplement their income particularly during lean farming periods) and palm wine tappers were found to be the most knowledgeable about pangolin ecology and biology since they serve as the primary source in the harvest and distribution of pangolins in this bushmeat commodity chain. In

Ghana, only farmer hunters were selected while both farmer hunters and palm wine tappers were selected in Sierra Leone because they were the main stakeholders that hunt pangolins.

Local Ecological Knowledge of pangolins was recorded from 279 interviewees using a semi- structured questionnaire and methods suggested by Hay (2000) where individual interviews were conducted on a one-on-one basis in a semi-structured manner and encouraging respondents to speak freely about their experiences and knowledge concerning pangolins. Of the interviewees, 42 palm wine tappers and 84 farmer hunters were interviewed in Sierra

Leone while 153 farmer hunters were interviewed in Ghana. The majority of the interviews were open-ended while some questions were coded using a Likert scale and participants were offered the opportunity to elaborate when necessary. Respondents were also afforded the opportunity to answer “not sure” if they could not answer a question in order to avoid speculative answers. All informants were shown photographs of the three pangolin species occurring in Ghana and Sierra Leone and were asked if they could recognize the species, what the local name for that species was, and whether they had personally hunted it before.

The ecological questions related to the habitat, diet, and relative abundance of each pangolin species while the biological questions related to the gestation period, the date that young are born, number of birthing events per year, number of offspring per birthing event and longevity of pangolins in the wild as well as in captivity. Participants were also asked about taboos associated with hunting or the cultural use of pangolins, their conservation status and laws relating to their protection. Demographic data of participants were also collected.

6.3 Data analysis

All statistical analyses were performed in STATISTICA 12 (StatSoft Inc., 2013). A Kruskal-

Wallis analysis was used to test for associations between interviewee age groups as well as years of hunting experience of participants and their response to birth frequency as well as litter size of pangolins.

6.4 Results

The majority of participants from Ghana were above 40 years of age while the majority of participants from Sierra Leone were between the ages of 31 and 40 years (Table 6.1). Of the

42 palm wine tappers interviewed in Sierra Leone, 64% (n=27) were between the ages of 31 and 40 years. All participants were male.

Table 6.1: Demographics of the people interviewed in both Ghana and Sierra Leone

Ghana

Age group of respondents Total number

Region 21-30 31-40 41-50 51-60 Above 60 of respondents

Eastern 3 6 10 10 12 41

Ashanti 2 5 10 9 14 40

Brong Ahafo 2 4 10 8 8 32

Central 0 3 8 5 7 23

Western 2 2 5 5 3 17

Total 9 20 43 37 44 153

Sierra Leone

Age group of respondents Total number

of respondents

District 21-30 31-40 41-50 51-60 Above 60

Bombali

Palm wine tappers 5 20 5 0 0 30

Farmer hunters 2 3 4 3 4 16

Kenema

Palm wine tappers 0 4 2 0 0 6

Farmer hunters 17 7 5 4 6 39

Kailahun

Palm wine tappers 1 3 2 0 0 6

Farmer hunters 7 4 4 7 7 29

Total 32 41 22 14 17 126

6.4.1 General morphological characteristics

All respondents were able to identify and were familiar with both black-bellied (P. tetradactyla) and white-bellied pangolins (P. tricuspis) from photographs presented to them.

The shape and texture of the scales as well as belly colour were the most easily identifiable morphological characteristics used by respondents to distinguish between black-bellied and white-bellied pangolins. All participants agreed that the scales of white-bellied pangolins were brown, smaller and softer than the black-bellied pangolin which has larger, harder and dark brown scales that are yellowish at the edges. All participants described the white-bellied pangolin as having sparse white hairs on the belly while the black-bellied pangolin has coarse black hair on their belly. Participants also agreed that the tail of the black-bellied pangolin is longer than that of the white-bellied pangolin. Local name for pangolin in Ghana is Apraa within the Akan geographic area that data was collected. In Sierra Leone, pangolin is referred to as shame beef in the Krio English, Mbata by the Temne and Limba tribe and Khanyilo by the Mende tribe where data collection was undertaken.

6.4.2 General ecology and diet

All respondents in Ghana mentioned that both pangolin species are arboreal and sleep or rest mainly in tree hollows or in holes beneath the tree trunk and that their diet consists entirely of ants and termites (100%, n = 153) , oil palm fruit (Elaeis guineensis) (60%, n = 92) and cassava (Manihot esculenta) (32%, n = 49). With regards to the number of respondents that mentioned oil palm fruit as diet for pangolins, the Eastern region had the highest number of respondents (33%, n = 30) while the Ashanti region had the highest number of respondents that mentioned cassava as an alternative diet for pangolins (43%, n = 21) (Figure 6.2).

Regarding age group, the highest number of respondents that mentioned oil palm fruit was above 60 years (29%, n = 27) and between 41-50 years of age (33%, n = 16) for cassava.

Figure 6.2: Age group and regional response to alternative diet for pangolins in Ghana

All hunters questioned in Sierra Leone (n = 126) stated that pangolins are arboreal and sleep or rest predominantly in holes in oil palm trees and feed on ants (100%, n = 126) and oil palm fruit (100%, n = 126) but none of them mentioned termites. Protected forests and farm/bush environments on farms were mentioned as the primary habitat for pangolins by all respondents.

6.4.3 Temporal relative patterns of abundance

Knowledge about relative abundance of species did not differ among participants with all agreeing that white-bellied pangolins are more frequently sighted and caught than black-

98 bellied pangolins in both countries. In relation to seasonal sighting, all respondents stated that pangolins are more likely to be sighted and caught in the dry season (November to April) than the rainy season (May to October). Regarding capture and trapping methods, all participants mentioned snares ahead of a shotgun and active searching.

6.4.4 Reproductive biology

None of the participants in either country knew at what age pangolins reach sexual maturity or the length of their gestation period. Respondents in Ghana stated that pangolins in a year give birth once (52%, n = 80), twice (44%, n = 67) and not sure (4%, n = 6). With regards to litter size in Ghana, 68% (n = 104) stated one, 24% (n = 36) stated two and 6% (n = 13) stated not sure. In Sierra Leone, respondents indicated that pangolins in a year give birth once

(17%, n = 7), twice (83%, n = 35) with no record of not sure for palm wine tappers and once

(50%, n = 42), twice (37%, n = 31) and not sure (13%, n = 11) for farmer hunters. Litter size per female for palm wine tappers were recorded as one (98%, n = 41), two (2%, n = 1) with no mention of not sure while farmer hunters mentioned one (29%, n = 24), two (30%, n =

25), and not sure (41%, n = 35) in Sierra Lone.

Participant’s response with respect to age group as well as stakeholder groupings to birth frequency and litter size is presented in (Figure 6.3). The majority of the palm wine tappers that mentioned birth frequency as once and litter size as one were within the age group of 31 and 40 while the majority of farmer hunters within the age group of 21 and 30 mentioned birth frequency as once but were not sure of litter size in Sierra Leone (Figure 6.3). In Ghana, birth frequency of once and litter size of one were the highest number of response and were both found for participants above 60 years (6.3). There were no significant differences

99 between respondents to birth frequency (KW = 2.05, P < 0.73) and litter size (KW = 3.51, P

< 0.45) in Ghana as well as in Sierra Leone birth frequency (KW = 1.70, P < 0.79) and litter size (KW = 2.30, P < 0.68).

Figure 6.3: Birth frequency and litter size response among palm wine tappers (PWT), farmer hunters in Sierra Leone (FHSL) and farmer hunter in Ghana (FHGH)

All participants in both countries agreed that pangolins can be domesticated but none of them had kept a pangolin beyond one week due to the high demand for domestic trade primarily for bushmeat consumption. None of the participants had successfully bred pangolins in captivity.

6.4.5 Cultural and conservation issues

Pangolins were not regarded as a totem species for any of the tribes interviewed. Of the three major tribes (Limba, Temne and Mende) interviewed in Sierra Leone, only the Mende had a

100 taboo associated with hunting pangolins in that when the animal rolls up into a defensive posture it means that it “likes” you and can therefore be collected but if it runs away it must be left alone. In Ghana, there were no taboos associated with the hunting and eating of pangolins among the Akan tribe and Northern tribes who have settled in the forested areas and often hunt pangolins. The Temne participants mentioned that the meat was used for treating stomach disorders while the Mende participants indicated that the meat is also used in the treatment of convulsion in children. In addition, participants agreed that the meat is usually reserved for chiefs but were not sure whether it was for medicinal purposes or as a delicacy. All participants in Ghana and Sierra Leone were aware of the closed hunting season for wild animals including pangolins but none were aware of the conservation laws pertaining to pangolins. Pangolins are completely protected in Ghana and no individuals may be hunted, killed or traded (Act 43: Wild Animals Preservation Act, 1961) but only the pups of white- bellied and black-bellied pangolins are protected in Sierra Leone (The Wild Life

Conservation Act, Act no. 27 of 1972).

6.5 Discussion

The morphological descriptions provided by LEK with regards to the shape, texture and colour of pangolin scales in addition to the belly colour and tail length descriptions were consistent with what is known in the scientific literature (Rahm, 1956; Gaubert, 2011;

Kingdon & Hoffman 2013). Respondents described holes in trees as resting or sleeping places for pangolins which is also similar to published ecological findings (Kingdon, 1971;

Haltenorth & Diller, 1980; Sodeinde & Adedipe, 1994; Akpona, Djagoun & Sinsin, 2008,

Gaubert, 2011; Kingdon & Hoffman, 2013). This indicates that participants are suitably familiar with these two pangolin species and their habits. Furthermore, this level of accuracy

101 may reflect frequent encounters with pangolins in tree holes during their hunting activities.

Palm trees have also been mentioned as resting or sleeping places for pangolins by hunters in south-western Nigeria (Sodeinde & Adedipe, 1994). The Local Ecological Knowledge from this study is the first record of African pangolins being located in exotic oil palm trees, although records of pangolins in oil palm trees has been established in scientific literature

(Maddox et al., 2007; Gaubert, 2011).

LEK findings that ants and termites are the primary diet for pangolins are consistent with previous published scientific literature (Kingdon, 1971; Haltenorth & Diller, 1980; Sodeinde

& Adedipe, 1994; Akpona, Djagoun & Sinsin, 2008; Gaubert, 2011; Kingdon & Hoffman,

2013). The occurrence of termites in epiphytic ferns and the forest canopy is known to be lower than their occurrence in the litter in oil palm plantations (Turner & Foster, 2009;

Ogedegbe & Ogedegbe, 2014). This may account for the lack of LEK about termites as a prey item of pangolins by respondents in Sierra Leone since all the respondents hunt pangolins from palm trees where termite occurrence and biomass is low. Local Ecological

Knowledge with regards to pangolins foraging on oil palm fruit and cassava has not been previously recorded and may provide new insights that require further investigation.

Agricultural production, particularly the farming of oil palm and cassava (Angelucci, 2013a, b) within regions where interviews were conducted, did have an influence on the presumed alternative diet for pangolins. It remains unclear, but is highly unlikely, whether pangolins are utilising the fruit but more likely attracted to ant species that are attracted to these fruits as ant abundance and density has been found to be higher in the canopy of oil palm trees compared to the surrounding vegetation (Pfeiffer, Tuck & Lay, 2008; Turner & Foster, 2009; Fayle et al., 2010; Luke et al., 2014; Ogedegbe & Ogedegbe, 2014). Ant numbers have also been found to be higher in cassava plantations in forested zones (Cudjoe, Neuenschwander &

102

Copland, 1993; Agboton et al., 2006). The possible misconception that pangolins actually forage on these agricultural fruits has led to their demise as a form of pest control by oil palm plantation farmers interviewed in the Kailahun and Kenema Districts of Sierra Leone. Similar misconceptions relating to other species such as geckos being labelled as venomous and carriers of diseases in LEK have resulted in their persecution and near demise in southern

Portugal (Ceríaco et al., 2011).

Although respondents in this study claimed to have caught black-bellied pangolins, the consensus is that this species is less frequently sighted than the white-bellied pangolin. This is consistent with other studies undertaken in south-western Nigeria (Anadu, Elamah &

Oates, 1988; Sodeinde & Adedipe, 1994) and in the Niger Delta (Haltenorth & Diller, 1980) in that white-bellied pangolins were the most commonly caught species while black-bellied pangolins are considered rare by hunters. In addition, no respondent reported sighting or hunting giant ground pangolins in this study which was also the case in south-western Nigeria

(Anadu, Elamah & Oates, 1988; Sodeinde & Adedipe, 1994). The status of the giant ground pangolin in West Africa in general needs to be ascertained since studies on mammal populations in Ghana (Yeboah, 1998; Vordzogbe, Attuquayefio & Gbogbo, 2005), Nigeria

(Angelici, Egbide & Akani, 2001), Sierra Leone (Lindsell, Klop & Siaka, 2011) and Liberia

(Barrie et al., 2007; Bene, Gamys & Dufour, 2013) have failed to record this species. A seminal work on pangolins in the Ivory Coast by Rahm (1956) did not record the giant ground pangolin either and evidence of their existence in this country was only from scales and a piece of skin within communal markets. In addition, Schulte-Herbrüggen et al. (2013a) did not mention giant ground pangolins among species of pangolins hunted for bushmeat purposes in Ghana. As such, LEK may serve as a valuable tool in assessing distribution

103 through the sighting of certain species throughout Africa where they once may have occurred but have subsequently declined or disappeared altogether.

This study found that pangolins were more readily sighted during the dry season (November-

March) than the rainy season (April-October) and is similar to the findings from hunters in south-western Nigeria (Sodeinde & Adedipe, 1994). However, LEK of hunters with regards to pangolin frequency of sighting may be related to the time and season invested into hunting as the dry season is the peak hunting period in Central and West Africa (Brashares et al.,

2011; Schulte-Herbrüggen et al., 2013a,b). In addition, this period also represents a time of increased human activity in palm groves for harvesting and corresponds to an increase in pangolin encounters in Sierra Leone (Lebbie & Guries, 2002). As in this study, snares are also the preferred hunting technique for pangolins in Vietnam (Newton et al., 2008) and

Equatorial Guinea (Fa & Gracía Yuste, 2001, Fa, Ryan & Bell, 2005).

Pangolins are described as elusive due to their shy, solitary and nocturnal nature in addition to sheltering in obscure burrows or holes in trees (Kingdon, 1971; Swart, Richardson &

Ferguson, 1999; Gaubert, 2011; Kingdon & Hoffman, 2013). In addition, pangolins are known to rotate between burrows which are often several meters deep (Kingdon, 1971;

Gaubert, 2011). As such, their elusive nature reduces their encounters with humans making aspects of their life history such as reproduction and true estimates of population density difficult to record. These factors may account for the variation in responses by respondents to their reproductive biology. Knowledge regarding the birth of a single pup at a time was similar to hunters questioned in the Democratic Republic of the Congo (Douglas, 1957),

Zimbabwe (Anchors, 2002) and Tanzania (Walsh, 2007) and was also consistent with reports

104 in the literature (Kingdon, 1971; Haltenorth & Diller, 1980; Gaubert, 2011; Kingdon &

Hoffman, 2013).

6.6 Conservation implications

Biodiversity surveys have not managed to comprehensively report on pangolin distribution and population densities in Africa and, when available, these reports are estimates at best.

Species-specific pangolin surveys to determine the population distribution and status as well as key areas and focal habitats for each African species have long been suggested by

Duckworth, Salter and Khounboline (1999). As such, local ecological knowledge still remains a useful tool in expanding the sources of biological information (Hunn, 2014), particularly for pangolins considering that Temminck’s ground pangolin (Smutsia temminckii) remains the only African pangolin species for which reliable ecological data exists (see Pietersen, McKechnie & Jansen, 2014b).

Although LEK may be available for specific species, suitable scientific surveys are needed to validate this since such LEK may not be relevant or sufficient to provide information useful enough to promulgate wildlife conservation management plans (Gilchrist, Mallory & Merkel,

2005). However, robust scientific surveys are needed to measure, verify and record the fundamental and basic biological characteristics of African pangolins since LEK provides limited usable biological and ecological information to formulate sustainable conservation management decisions for the species.

The lack of negative folklore and any traditional belief system prohibiting the use of pangolins also contribute to the threat to pangolin conservation as no cultural system is in

105 place to prevent harvesting. Many traditional beliefs in the form of taboos can contribute towards the protection of certain species by specific cultures (Meyer-Rochow, 2009; Jimoh et al., 2012). Conversely, totem species have been found to exert significant influence in conservation by forbidding tribal, clan or group members from hunting such species for any purpose (Saj, Mather & Sicotte, 2006, Dagba, Sambe & Shomkegh, 2013). Pangolins are not considered as a totem by any of the local people interviewed in this study, nor are there any taboos associated with eating or using them for medicinal purposes. Rather, public education about the potential loss of pangolins to an ancient African cultural system may be an important starting point in African pangolin conservation as this group of mammals are now considered the most traded and poached mammals globally (Challender, Waterman & Baillie,

2014).

6.7 Conclusion

The contribution of LEK on African pangolins was found to be minimal in providing the fundamental biological traits such as reproductive seasonality, maturation and fecundity that is required in order to make informed decisions regarding sustainable harvesting. LEK may serve as a valuable tool in assessing the distribution of certain pangolin species where they once may have occurred but have subsequently declined or disappeared altogether by frequency of observation at the local level. Scientific data is urgently required to garner more information on the finer biological and life history traits of a species such as reproductive biology, feeding preferences, habitat use and population abundance in order to provided suitable conservation management strategies and to estimate what a sustainable harvesting may entail. Biodiversity conservation objectives cannot be achieved without incorporating human dimensions, as such, it is important to continuously explore the cultural beliefs and

106 values that can assist in the development of pangolin conservation management plans thus making LEK an important means of generating local support for conservation efforts.

107

CHAPTER 7

SYNTHESIS

The overarching objective of this thesis was to investigate the use of pangolins for traditional medicinal purposes (Chapters 3-4) and the extent of their bushmeat trade (Chapter 5) in west

Africa. Following these investigations, the local ecological knowledge of hunters who serve as the primary source of pangolins for both traditional medicinal purposes and bushmeat were determined through interviews in order to ascertain their level of understanding of the ecology and reproductive biology of these elusive animals in addition to their whereabouts and habitat preferences (Chapter 6). From the results of this study, some future research recommendations are suggested that is deemed necessary for the conservation of African pangolins.

Some animal species and their specific body parts are consistently used more than others

(Cunningham & Zondi, 1991). The selective use of animals and their body parts can be attributed to the cultural importance attached to these species by the community or traditional healers. Following this, informant agreement ratio, use values and use agreement values were determined for whole animals or pangolin body parts to determine their cultural importance and significance. These indices are a quantitative method that demonstrates the relative importance of medicinal resources known locally and their application is based objectively on the importance attributed by the informants and does not depend on the opinion of the researcher (Alves & Rosa, 2006; Thomas et al., 2009; Alves et al., 2012). Various publications have shown the importance of pangolins in traditional medicine for the treatment of various ailments as well as spiritual conditions in Africa and Asia in particular. The scales have been identified as the most heavily exploited pangolin body part for traditional

108 medicinal purposes (Soewu & Sodeinde, 2015). In this study, the scales were found to be the most medicinally versatile and culturally significant pangolin body part used for medicinal purposes in both Sierra Leone and Ghana (Chapters 3 and 4).

The bushmeat commodity chain was investigated to better understand the extent of the pangolin bushmeat trade. The strength of the commodity chain approach is that it emphasizes the fundamental importance of identifying the participants involved in the trade and the roles that they play within this trade (Raikes, Jensen & Ponte, 2000). By following and investigating the chain of interactions along the bushmeat commodity chain (Chapter 5), the dynamics of each level of trade have been now recognised that was previously not investigated. The bushmeat commodity chain has already been investigated extensively in

Ghana looking into the trade of other mammals (Mendelson, Cowlishaw & Rowcliffe, 2003;

Cowlishaw, Mendelson & Rowcliffe, 2004; Cowlishaw, Mendelson & Rowcliffe, 2005a, b) such as the African straw-coloured fruit bat (Eidolon helvum) trade that also did not follow the established bushmeat chain (Kamins et al., 2011). The pangolin bushmeat trade was similar in that it also does not follow the typical major bushmeat market system that is common for bushmeat trade in Ghana. Additionally, Chapter 5 revealed that the pangolin bushmeat trade in Ghana was not geared towards the major bushmeat markets resulting in the underestimated level of trade thus having a larger impact on the threat to existing pangolin populations from the bushmeat trade.

Biodiversity conservation cannot be achieved without exploring all dimensions that govern the interactions between human societies and natural resources (Alves, 2012; Alves &

Albuquerque, 2012). Local ecological knowledge is therefore critical in understanding resource use and in the development of local and regional conservation policies. Biodiversity

109 surveys have not managed to comprehensively report on African pangolin distribution and their population status as well as identifying key areas and habitats for the conservation of each species (Duckworth, Salter & Khounboline, 1999). Currently, very little is known about the distribution and ecology of hunted pangolins in African forests (Challender et al., 2014).

However, this information is potentially available within Africa’s rural communities and can be provided through local ecological knowledge (Chapter 6), which has been a useful tool in expanding the sources of ecological information. However, this study found this knowledge to be somewhat rudimentary and cannot be used with any level of accuracy with regards to the species specific biology such as reproductive behaviour.

Considering the symbolic importance of pangolins to the culture of some tribes in Africa and their prevalent use in traditional medicine and bushmeat, it is vital to know with more accuracy their population distribution and abundance if the species is to be used sustainably

(Still, 2003; WHO, 2003; Alves, Rosa & Santana, 2007; Alves, Souto & Barboza, 2010).

Currently, there are no population density estimates or ecological studies on either

Phataginus tetradactyla or Smutsia gigantea (IUCN, 2014). Most of the research on population densities and distribution range of African pangolins have been undertaken on the

Temminck’s Ground Pangolin in southern Africa (Smutsia temminckii) (van Aarde,

Richardson & Pietersen, 1990; Jacobsen et al., 1991; Heath & Coulson, 1997; Swart,

Richardson & Ferguson, 1999; Pietersen, McKechnie & Jansen, 2014b) and a single base-line study for Phataginus tricuspis in Benin (Akpona, Djagoun & Sinsin, 2008). Furthermore, there is a total lack of scientific information on African pangolin biology such as reproductive behaviour, recruitment, mortality and habitat use with such studies limited to Smutsia temminckii in southern Africa (Heath & Coulson, 1997; Swart, Richardson & Ferguson,

1999; Pietersen, McKechnie & Jansen, 2014b). Considering that population trends for all four

110

African pangolin species are rapidly declining (IUCN, 2014), this study strongly recommends that ecological research be undertaken to determine the current population densities and distribution of pangolins in Africa.

111

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APPENDIX 1

QUESTIONNAIRE

Faculty of Science

Department Environmental, Water and Earth Sciences

THANK YOU FOR YOUR WILLINGNESS TO COMPLETE THIS QUESTIONNAIRE.

The purpose of this questionnaire is to look at pangolin use as a source of bushmeat and for traditional medicinal purposes, and the implications of this use for conservation of these species. The researcher will like to propose a realistic response to conservation of this threatened group, it is therefore necessary to understand better the relationship between their use as a source of bushmeat and their medicinal value as dictated by cultural and traditional values.

It is important that you answer all questions as honestly and directly as possible.

Your answers to this questionnaire will be treated as confidential. The completed questionnaires will only be seen by the researchers and will be locked in a safe until destroyed.

Tel. 0861 102 422, Tel. (012) 382-5911, Fax (012) 382-5114, www.tut.ac.za • The Registrar, Private Bag X680, Pretoria 0001

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You are requested NOT to reveal your own identity.

Complete the questionnaire by circling the appropriate number in the shaded box or by answering the question/statement in the space provided.

Field Data Sheet

Date: Country: Region/State/Province:

Time: Town: Respondent Number:

Section A: Respondent Information

1. Stakeholder grouping

Traditional medical practitioner 1 Wholesaler of wildlife 2

Retailer of wildlife 3 Commercial hunter 4

Farmer hunter (collector) 5 Restaurants operator 6

Middleman 7 Exporter 8

Other (specify):

2. Sex Male Female

3. Age group 15-20 21-30 31-40 41-50 51-60 Above 60

4. Number of years in business (trade) 1-2 3-4 5-10 11-15 16-20 Above 20

5. Time involved in business (trading) activity Full time Part time

6. Ethnicity/Tribe

7. Religion Christian Muslim Animist Others

8. Last level of Below Below Secondary Post-secondary Quoranic education primary secondary

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9. Purpose of collecting/using Traditional Medicine Bushmeat Trade Others

pangolin

Section B: Price and availability

1. What is the average price of a pangolin?

2. Average price of an adult/big pangolin?

3. Average price of a young/small pangolin?

4. Price fluctuations within the last year Increase Decrease Stable Not Sure

5. Reason(s) for price fluctuation?

…..……………….………………………………………………………………………….

6. Is there any seasonal (dry/rainy) variation in price of pangolins? Yes No

7. If your answer to question 6 is yes, which season is more expensive? Dry Rainy

8. Reason(s) for the high price during that season?

………......

Section C: Traditional Medicinal Knowledge

1. How did you learn about animal therapeutics? Oral folklore Apprenticeship

2. How do period of political crises or conflict Increase Decrease Stable Not Sure

affect use of pangolins for traditional medicine?

3. How do period of economic crises affect use Increase Decrease Stable Not Sure

of pangolins for traditional medicine?

4. How do period of festivities (traditional, Increase Decrease Stable Not Sure

Christmas, Sallah) affect use of pangolins for

traditional medicine?

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5. Is there any variation in seasonal (dry/rainy) use of pangolins Yes No for traditional medicinal purpose?

6. If your answer to question 5 is yes, which season is highest? Dry Rainy

7. Reason(s) for the high usage? ......

8. What are the traditional medicinal uses of pangolins (whole or parts)?

Sex (M/F) Parts used Conditions used to treat

Species used

Tree or African White-bellied Pangolin

(Phataginus tricuspis)

Long tailed or Black-bellied Pangolin

(Phataginus tetradactyla)

Giant Ground Pangolin (Smutsia gigantea)

Section D: Bushmeat Trade

1. Do you eat pangolin as a source of bushmeat? Yes No

2. What pangolin species do they eat regularly? (indicate by preference-1,2,3)

Tree or African White-bellied Pangolin (Phataginus tricuspis)

Long tailed or Black-bellied Pangolin (Phataginus tetradactyla)

Giant Ground Pangolin (Smutsia gigantea)

3. Do you have an idea where your suppliers get their Yes No catch?

4. If answer to question 3 is yes mentions place(s)…………………………………………

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5. Trend in number of pangolins Increase Decrease Stable Not Sure captured/traded within the last year

6. Reason(s) for fluctuation?

………………………………………………………………………………………………

7. How many pangolin collectors supply you?

......

8. Have you received any of the following animals from your suppliers before?

Species How often? (supply frequency)

Yes No Weekly Monthly Irregular

Tree or African White-bellied Pangolin

(Phataginus tricuspis)

Long tailed or Black-bellied Pangolin

(Phataginus tetradactyla)

Giant Ground Pangolin (Smutsia gigantea)

9 Average number of pangolins (by species) captured/brought to you at a go within the past week.

…......

10. Where to find pangolins on sale Markets Hunter Road side Others

(where are they sold)?

Section E: Traditional Ecological Knowledge

1. Where are pangolins usually found? …………………………………………………..

2. Do you know the breeding season of pangolins? Yes No

3. How frequent does it give birth Monthly Yearly Not Sure

4. How many offspring per time One Two Not Sure

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5. What is their diet?

6. Time of day when easy to sight Morning Afternoon Evening Night

7. Season when easy to sight Dry Rainy

8. Capture Trapping Hunting (dog) Hunting (gun) Poisoning Others

technique

9. Are there any taboos associated with hunting pangolins? Yes No

10. If your answer to question 9 is yes, explain the taboo(s)

11. What is the traditional use of pangolin if any?

Section F: Conservation status

1. Do you think the pangolins will be extinct? Yes No

2. If Yes, how many years do you predict this will happen?

3. What factors do you think are the major cause of this extinction?

4. Are there sacred places where the capture of pangolin is forbidden? Yes No

5. Do you know of any laws that regulate their capture and use both for Yes No

traditional medicinal purpose as well as bushmeat?

6. Do you think laws are needed to regulate their capture and use both Yes No

for traditional medicinal purpose as well as bushmeat?

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