Assessing Africa-Wide Pangolin Exploitation by Scaling Local Data

Introduction

Overexploitation is one of the main pressures causing species’ declines and local extinctions (Maxwell et al. 2016; Ducatez & Shine 2017). Currently, broad-scale data on the exploitation of terrestrial wildlife, needed to inform conservation policy and action, are lacking (Joppa et al. 2016). Information on wildlife harvests can be difficult to collect because, at times, hunters and traffickers operate secretly to avoid law enforcement, and may be unwilling to disclose what they have harvested (Keane et al. 2008). Law enforcement and seizures data have been used to quantify exploitation of threatened species; however, these data suffer from detection biases and underestimation (Gavin et al. 2010). Instead, collating local-scale hunting studies may provide more accurate estimates of the number of animals hunted and relevant information to aid conservation efforts, complementing seizures data (Sánchez-Mercado et al. 2016).

Pangolins (Family: Manidae), a group of African and Asian scaly mammals, are considered to be “the most heavily trafficked wild mammal in the world,” and are hunted and traded for food and traditional medicines (Challender et al. 2014). They are also used in rituals, art, and magic among communities across Africa (Soewu & Sodeinde 2015) and Asia (e.g., Mahmood et al. 2012). Despite a long history of exploitation, pangolin populations in Asia have declined dramatically (estimated 90% decline of Chinese pangolin [Manis pentadactyla] since the 1960s; Wu et al. 2004). All four Asian pangolin species are listed as “Critically Endangered” or “Endangered” on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species due to past, present, and predicted population declines driven by growing demand for meat and scales (Challender et al. 2014), and compounded by low reproductive rates (Newton et al. 2008; Challender et al. 2012; Cheng et al. 2017). In addition, commercial trade and international trade of wild-caught pangolins has been banned (CITES 2016).

In comparison to Asian pangolins, less is known about the African species: white-bellied (Phataginus tricuspis), black-bellied (Phataginus tetradactyla), giant ground (Smutsia gigantea), and Temminck's ground pangolin (Smutsia temminckii). They are currently classified as “Vulnerable” by the IUCN (Pietersen, Waterman et al. 2014; Waterman et al. 2014a,b; Waterman, Pietersen et al. 2014), and international trade was recently banned (CITES 2016). African pangolin populations are assumed to be declining, because of habitat degradation and loss (Challender et al. 2014), hunting, and increasing demand from international markets (Challender & Hywood 2012). However, little is known about population sizes, reproductive potential, and African pangolin trade. Mounting evidence suggests that as the availability of Asian pangolins declines and international trade flows increase, traders are increasingly supplying the currently more abundant and less expensive African pangolins to meet Asian demand (Challender & Hywood 2012).

Seizures of pangolins and their derivatives (e.g., scales and skins) from Africa destined for Asia are increasing (Heinrich et al. 2016) with over 53 tons seized in 2013 (Flocken 2015), and more than 1 million pangolins trafficked globally since 2000 as estimated from illegal trade data (IUCN SSC Pangolin Specialist Group 2016). These estimates likely represent a fraction of all pangolins traded, and an even smaller proportion of the number of pangolins hunted.

Many studies have monitored wildlife hunting and/or markets at local scales across Africa (e.g., Crookes et al. 2006; Coad et al. 2013). Collating data from these studies allows us to infer trends, produce indicators of overall rarity and demand at a regional scale, and provide information to aid conservation efforts. Here, we collate data from local-scale hunting and market studies to provide the first comprehensive assessment of the exploitation of African pangolins by estimating: (1) the total number of pangolins hunted annually; (2) temporal trends in the proportion of pangolins of all animals hunted or observed at wild meat markets; and (3) trends in the price of pangolins over time as an indicator of changes in demand or rarity (Courchamp et al. 2006).

Materials and methods

Results

Data

We collated data from 68 sources that met our inclusion criteria (Table S1), separated into 161 studies and 204 samples, accounting for 348,807 individual vertebrates. Of these, 152 samples had information on 71,716 individual vertebrates in the catch and 52 samples investigated 277,091 individuals at markets, of which 2,059 and 7,005 individuals were pangolins, respectively. Across all samples, 8,166 individuals were identified as arboreal pangolins (Phataginus sp.) and 300 as ground pangolins (Smutsia sp.), with a further 578 only identified to family (Manidae).

Pangolins were hunted at 71 of 113 (63%) sites in 10 of 14 (71%) countries, and observed at 18 of 36 (50%) markets in all seven countries for which we have data (Figure 1). On average, over time and across countries, per sample, pangolins represented 2.1 ± 0.27% (mean ± SE) of vertebrates in the catch and 1.4 ± 0.23% at markets.

The sex composition of pangolins in the catch was 49% female, 45% male, with 6% of unknown sex (n = 560 pangolins from 10 sources). Most (50%) were adults, 45% juveniles and subadults, and 5% of unknown age (n = 310 pangolins, 5 sources). Pangolins were hunted by traps and snares (54%), hand (25%), gun (16%), or other means (5%) (n = 822 pangolins, 14 sources). Pangolins were either directly consumed (50%), sold (41%), or given as gifts (9%) (n = 425 pangolins, 9 sources).

Estimating total catch of pangolins in Central African forests

We estimate that between 0.42 and 2.71 million pangolins (Phataginus spp. and S. gigantea) were hunted each year in Central Africa (sampled range 1975-2014), with the two human population-based methods giving higher estimates of 1.68 million (0.22-4.76 interquartile range) and 2.71 million (0.35-7.66) pangolins (Figure 2; Table S1 and Figure S2). The total annual catch of pangolins has increased by an estimated 145-151% from before 2000 (range 1975-1999) to post-2000 (2000-2014) depending on estimation method (Figure 2). S. temmickii does not occur in Central African forests, and insufficient data were available to estimate total annual catch where it occurs.

Trends in pangolins hunted and observed at markets

The percentage of pangolins in the catch increased significantly from 0.04% in 1972 to 1.83% in 2014 (Figure 3A, minimum adequate model: percentage of pangolins = year + random effects of StudyID nested within SourceID, and Country, χ²_5,6 = 6.4, P = 0.012). For comparison, we also found no temporal trends for the main hunted taxonomic groups (Cetartiodacyla and Rodentia; Figure S3), but we did find that pangolins account for more of the catch in the most accessible areas (Figure S4). The percentage of pangolins observed at markets did not change significantly between 1975 and 2010 (Figure 3B; χ²_4,5 = 1.9, P = 0.17).

Trends in price

We collated price data for arboreal (n = 149 records) and giant ground (n = 32) pangolins from 31 sources in five countries. Prices for arboreal pangolins changed significantly over time, and changes differed depending on market type (Figure 4A, interaction: χ²_6,8 = 8.0, P = 0.02; urban markets increasing from ∼3,700 to 8,500 Central African Francs [CFA] and rural markets decreasing slightly from 3,200 to 2,700 CFA). The price of giant ground pangolins increased significantly at urban markets between 1993 and 2014 from approximately 24,000 to 140,000 CFA (Figure 4B: χ²_3,4 = 3.9, P = 0.05), but not in rural ones where we have few prices (n = 8).

We calculated price ratios for blue duikers (n = 134 price records), brush-tailed porcupines (n = 134), and cane rats (n = 82) based on data from 31 sources collected at 85 sites in five countries between 1992 and 2014 (Table S1). Price ratios of arboreal pangolins to blue duikers increased significantly in urban markets (0.024 ± 0.008 ratio increase per year ± SE, Figure 5A, Figure S5), and decreased in rural markets (-0.017 ± 0.007 ratio decrease per year; interaction of year and market type, χ²_5,6 = 12.9, P = 0.0003). We found no significant interaction of year and market type for the price ratio with porcupines (χ²_5,6 = 3.0, P = 0.08) or cane rats (χ²_5,6 = 0.06, P = 0.81), or any effect of year on the price ratios for porcupines (χ²_3,4 = 0.03, P = 0.87) or cane rats (χ²_3,4 = 0.01, P = 0.93).

Discussion

By collating local-scale studies, we provide the first regional estimates of African pangolin exploitation, revealing that pangolins are hunted and observed at markets throughout West and Central Africa, and that pressure from hunting has increased. The proportion of pangolins in the catch increased significantly over time, while the proportion observed at markets remained unchanged. We found evidence that the price of whole pangolins increased significantly at urban markets, but not at rural ones.

We estimate that 0.4-2.7 million pangolins (P. tricuspis, P. tetradactyla, and S. gigantea) were hunted annually in Central African forests, based on forest area- or human population-based extrapolations of average hunting levels. Our area-based estimate of ∼420,000 pangolins hunted annually is consistent with a previous area-based estimate of ∼400,000 P. tricuspis, and ∼100,000 S. gigantea annually in Central Africa, although based on fewer studies and excluding P. tetradactyla (Fa & Peres 2001). Studies rely on the willingness of hunters to participate, so studies may represent only a subset of hunters at a particular site. Furthermore, hunters and traders may either fail to report illegally hunted protected species, or may not participate in studies; therefore, our extrapolations are likely conservative.

Our analyses suggest that the number of pangolins hunted has increased. Comparing forest area- or population-based extrapolations of data from before and after 2000, we found an ∼150% increase, although interquartile ranges overlap likely due to relatively small sample sizes. When analyzing hunting samples, the percentage of pangolins out of the total catch increased significantly from ∼0% to ∼2% over four decades. The percentage of pangolins observed at markets remained unchanged, suggesting pangolins may be traded along alternative supply chains as observed in Ghana where pangolins were often traded to wholesalers away from wild meat markets (Boakye et al. 2016), and in Gabon where Asian industry workers buy pangolins directly from hunters (Mambeya et al. unpublished). The reliability of market studies to assess exploitation has been questioned (Crookes et al. 2006) because individuals observed at markets likely represent a fraction of those hunted as traders hide illegal goods to avoid law enforcement. We cannot discern whether the observed increase in pangolins hunted is caused by: (1) increased consumption, (2) increased hunting of smaller mammals due to declines in larger species (Ingram et al. 2015), (3) changes in hunting technology, and/or (4) increased demand from international markets (Challender & Hywood 2012).

We provide evidence that current hunting of African pangolins is likely unsustainable. On average, 45% of individuals were either juveniles or subadults, an indicator of overexploitation (Weinbaum et al. 2013), although aging subadults is difficult and our assessment relies on the authors reporting of age. This is of concern because pangolins take up to 2 years to reach sexual maturity and produce only one pup annually (Soewu & Sodeinde 2015), suggesting many of the pangolins hunted had not reproduced. Traps and snares were the most common hunting method (54%), however, the use of wire snares is illegal in all pangolin range states because they are effectively “blind” to the species trapped, but law enforcers often ignore or tolerate snaring (LAGA 2015). Effective law enforcement is needed, and should include stricter controls of snaring, such as snare specialist teams (Gandiwa et al. 2013), the elimination of corruption, and the provision of alternative protein sources and incomes.

We found substantial price increases for giant ground pangolins at urban markets, which may suggest that early signs of increased demand may not yet have been passed down to rural hunters, or that prices are responding to increased demand that is unmet by hunters because of depletion. We found small increases in prices and price ratios for arboreal pangolins in urban markets that, while increasing slowly, appear to be following the increasing trend of prices in Asia (Newton et al. 2008). Anecdotal evidence suggests that rural hunters may not yet know the value of pangolins elsewhere (Mambeya et al. unpublished).

While CITES provides a mandate for sustainable international wildlife trade, recently banning trade of all pangolin species (CITES 2016), it does not provide enforcement mechanisms on the ground. To implement the trade ban, governments, law enforcement officials, and conservationists need to better understand the supply chains of pangolins from Africa and Asia, to implement an appropriate monitoring program, and to increase the capacity to enforce the ban and intercept illegal shipments. To better target and inform conservation efforts, tailored survey methods to accurately estimate pangolin abundance and collect vital ecological data are needed. In addition, efforts should focus on determining local demand, and when/where this leads to unsustainable hunting. For cases where pangolin hunting is unsustainable, efforts should be made to improve and increase domestic law enforcement, increase public awareness, reduce indiscriminate hunting methods such as snaring, and work with local communities to find effective solutions. Next steps should involve investigating harvests and enforcing legislations in support of country-wide conservation efforts. In addition, it is imperative that China, as one of the main consumers, considers implementation of awareness campaigns as well as increased monitoring, law enforcement, and penalties. Pangolins have attracted conservation attention recently, and as people become increasingly aware of the focus on pangolin hunting, the perceptions and stigmas of pangolin hunting are also likely to change over time.

Using African pangolins as a case study, we have demonstrated that collating local-scale data from hunting and market studies can be used to assess regional trends in wildlife exploitation. Local-scale data complement seizures data, by providing estimates of local demand and more accurate estimates of total hunting rates. Together, these types of data give insights into different aspects of pangolin use and trade, and paint a more complete picture of pangolin exploitation. In the absence of continent-wide species monitoring programs, collating local-scale data can highlight pressures on wildlife, and provide detailed quantitative information on wildlife exploitation that are crucial to inform conservation action and policy.