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 [8, 40]. The high UV for pangolin scales implies that the scales are extremely important to the traditional medical practitioners. Rossato et al. [41] 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. [15] 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 [19]. We 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 [15, 17, 19, 24, 25]. 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. We found a high use of pangolin scales for treating rheumatism which has also been mentioned in previous studies [15, 17, 19, 24] 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. [15] mentions that pangolin meat is less valued in terms of medicinal properties to other body parts, however, our study indicates that the meat was relatively important for the people of Sierra Leone ranking third in terms of its use value. However, 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 disuse disorders but it has also been reported to treat rheumatism within Nigerian tribal communities [17, 19]. 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. We found that the pangolin head was prescribed within 10 ICD categories, a great deal more than was found in similar studies undertaken in Nigeria by [17, 19]. 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 [24]. Also, studies in Nigeria indicate the entire animal can be prescribed for invisibility which we 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.
Informant agreement ratio (IAR)
The IAR values are a reflection of the extent and distribution of knowledge 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 [8, 45, 46]. 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. [47], 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 [44]. 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 [48]. 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.
Comparing different indices
Both the UV and IAR varied for different ICD categories. Thomas et al. [44] 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. [44], 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 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 [44] 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.
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 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 [49], 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 [50]. 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 [51, 52]. 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 anytime 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 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 [53].
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. To the best of our knowledge 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 [34]. 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 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 et al. [54] have identified the need to increase our 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 [17, 19] 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 [22, 34]. 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 as traditional medical practitioners about the implications of their medical practices on the wild population. 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 the wild population.