The CITES Trade Database holds a total of 2,129 trade records of ball pythons exported from range states, documenting total exports of between three and four million individual ball pythons (exporter-reported exports: 3,121,022; importer-reported exports: 3,979,680) since the first recorded export of the species in 1975. Since that time, 11 of 18 range states exported ball pythons but only six reached total exports over the period of 5,000 or more: Benin, Ghana, Guinea, Mali, Niger and Togo. The following numbers are based on importer-reported data but the relative ranking of range states as ball python exporters is the same regardless of the specific dataset used. Exports from Mali peaked in 1995 at 5,750, and comprised 14.2% of annual ball python exports that year, but <3% the following year, and <1% in all other years. Exports from Guinea and Niger comprised a small proportion of annual exports in all years, peaking at 3.6 and 2.1% (in 1997 and 2005, respectively). In total, through the 1980s, 1990s and 2000s, exports from Benin, Ghana and Togo collectively comprised 98.8% of all ball python exports from range states (28.6%, 44.0% and 26.2%, respectively; Fig. 1). Exports of ball pythons from Guinea, Mali and Niger were last recorded in 2008, 2010 and 2009 (respectively), and, since 2011, Benin, Ghana and Togo were the only range states to have reported ball python exports. Guinea and Liberia have been under a CITES trade suspension for all commercial trade since 2013 (CITES Notification No. 2019/075), and 2016 (CITES Notification No. 2018/012), respectively, as was Guinea-Bissau between 2016 and 2018 (CITES Notification No. 2018/011).

Export volume and trends

In total, CITES trade records document the export of approximately one million live ball pythons from each of Benin, Ghana and Togo, up to 2017, over 99% of which were intended for commercial use. Annual country-level exports varied between 100 and over 100,000 individuals with similar patterns among the three countries: peaking in the mid-1990s (but not in Ghana) and in the early- to mid-2000s (Fig. 1b, Fig. 2). However, over the most recent 15 years (2003 - 2017), there was a statistically significant decline in annual importer-reported exports in Benin (from 82,303 to 19,577 per year; trend=-3246, F_{1, 13} = 16.54, p = 0.001; Fig. 2a) and in Ghana (from 77,510 to 13,887 per year; trend=-6625, F_{1, 14} = 38.75, p <0.001; Fig. 2b), but not in Togo (trend=-1,021; F_{1, 13} = 1.48, p = 0.246) where annual exports averaged 54,800 per year but showed considerable fluctuation (SD = 14,296; Fig. 2c) (exporter-reported data were not used to assess recent trends due to missing data). Considering only exports in the most recent five years in which there were no missing data (2011–2015), and taking account of year effects, exports from Togo were statistically significantly higher (annual mean between 2011 and 2015 = 54,163) than from Benin (annual mean = 21,876; Tukey post-hoc test, p = 0.001) (but not Ghana: annual mean = 38,415; p = 0.078).

Figure 2.

Annual export volume (number of individuals) of live ball pythons from Benin (a), Ghana (b) and Togo (c), as reported by both importing and exporting countries. Note: missing exporter-reported data in some years in all three countries. Source: CITES Trade Database (http://trade.cites.org/).

Countries differed in their tendency to under- or over-report exports (exporter-reported quantities < importer-reported quantities and vice versa, respectively; χ² = 9.22, df = 2, p = 0.010, based on the frequency of cases) and in the absolute value of discrepancies between exporter- and importer-reported quantities (ANOVA: F_{2, 83} = 7.46, p = 0.001). Exports from Togo were statistically significantly more likely to be under-reported (exports under-reported in 75% of 32 years) than from Ghana (where exports were over-reported in 62% of 34 years; post-hoc pairwise comparison p = 0.006; Fig. 2a–c) and discrepancies in reported quantities from Togo were statistically significantly greater than from either Ghana (Tukey’s post-hoc test, p = 0.002) or Benin (p = 0.012). Exports from Benin showed no particular tendency to be under- or over-reported (50% of 20 years reported in both cases), and did not differ from Ghana in terms of the absolute value of reporting discrepancies (p = 0.989).

Source

Trade records from all three countries exhibited a switch from predominantly wild-sourced to predominantly ranched individuals (albeit in the absence of extensive wild-sourced exports from Ghana prior to the uptake of ranching; Fig. 3). In all three countries, since approximately 2003 (up to 2017), an average of >90% of annual country-level importer-reported exports (excluding seizures) were documented “ranched” (source code R, or “born in captivity” [source code F]) and an average of < 6% were documented “wild-caught” (source code W; Fig. 3). However, the proportion of wild-caught individuals exported (post-2003) varied annually (ANOVA: F_{1, 41} = 6.59, p = 0.014) and among countries (F_{2, 41} = 4.51, p = 0.017), with Ghana, specifically, exporting a greater proportion of wild-caught individuals (maximum 15.9%, equating to 15,592 individuals, according to importer-reported quantities) as compared to Togo (annual maximum 5.2%, equating to 3,165 individuals; Tukey’s post-hoc test, p = 0.012).

Figure 3.

Source of annual exports (export volume, number of individuals) documented by Benin (a), Ghana (b) and Togo (c), based on importer-reported quantities in the period 1990–2017 (source codes were not recorded prior to 1990), together with export quotas (dashed lines) for ranched and wild specimens as communicated to CITES. Source codes defined as follows (Lyons et al. 2017): “Ranched” (R) = Specimens of animals reared in a controlled environment, taken as eggs or juveniles from the wild, where they would otherwise have had a very low probability of surviving to adulthood; “Bred in captivity” (C) = Animals bred in captivity in accordance with Resolution Conf. 10.16 (Rev.) (i.e. where parents mated in a controlled environment and where the breeding stock was established in a manner not detrimental to the survival of the species in the wild, and maintained [under normal circumstances] without the introduction of specimens from the wild); “Born in captivity” (F) = Animals born in captivity (F1 or subsequent generations) that do not fulfil the definition of “Bred in captivity” in Resolution Conf. 10.16 (Rev.) (e.g., parents did not mate in captivity, or the breeding stock/operations did not meet CITES requirements); Wild (W) = Specimens taken from the wild. Further detailed graphs in Suppl. material 1. Source: CITES Trade Database (http://trade.cites.org/) and UNEP (2019).

All three countries (post-2003) used additional alternative source codes representing different captive production systems; however, only Togo used the source code F, reporting a total of 26,782 individual ball pythons born in captivity exported between 2014 and 2017. All three countries used the source code C (“captive-bred”) in the mid-1990s prior to the establishment of ranching (see Fig. 3); post-2003, use of this source code was limited (Fig. 3) but nevertheless accounted for up to 6% of Benin’s exports (captive-bred individuals from Benin cannot be seen in the graph due to the low numbers and missing data in intermittent years but amounted to 1,000 individuals in each of 2006, 2007 and 2008, 600 in 2011 and 2012, and 1,200 in 2017) and up to 20% of Ghana’s exports (in 2014, equating to 3,770 individuals).

U.S. Fish and Wildlife Service LEMIS import data listed a total of 51 unique export company names (inferred on the basis of similar spelling; n = 18, 22 and 11, respectively, in Benin, Ghana and Togo) that exported ball pythons to the USA between 2000 and 2017. Of the 51 export companies listed, only two to three (per country) operated in all years, and these were responsible for 64.8%, 71.8% and 88.3% (respectively, for Benin, Ghana and Togo) of total country exports to the USA. In Benin and Ghana, the number of export companies shipping ball pythons to the USA declined from eight and 11 in 2004 and 2005, respectively, to four and two in 2017. The number of export companies in Togo exporting to the USA in a single year was between two and six over the entire period (2000–2017; four in 2017).

Markets

CITES trade records document exports of ball pythons from Benin to 34 different countries/territories, and from both Ghana and Togo to each 57 different countries/territories (Suppl. material 2). The following is based on exporter-reported quantities. The USA was the largest importer from all three countries (Fig. 4). Over the most recent five years (2012–2016), the most significant importing countries/territories after the USA were: Hong Kong, the UK, France, Spain, and Ghana (albeit with each importing country/territory being the main importer for different exporting countries, Fig. 4). At a regional level, over the most recent five years, there was a statistically significant association between exporting country and importing regions (χ² = 65643, df = 8, p<0.001) such that Ghana appeared to be less dependent on the USA market than either Togo or Benin, exporting to a more diverse range of countries and, specifically, exporting significantly more snakes to Asian countries (36.6% exports compared with 6.8% and 10.4% for Benin and Togo, predominantly Hong Kong, but also Japan and Taiwan). Western European countries were prominent as importers from all three countries, comprising 9.1%, 18.3% and 15.1% of exports from Benin, Ghana and Togo, respectively (Fig. 4). There was little intra-continental trade within Africa originating from range states (except between Togo, Benin and Ghana, Fig. 4; see Trade links below). The only African non-range states to play a role as importers were Egypt (another major hub for the export of snakes from the African continent; see Jensen et al. 2019) and South Africa. Collectively, African countries were responsible for receiving only 6.4%, 1.5% and 3.7% of exports from Benin, Ghana and Togo.

Figure 4.

Countries importing live ball pythons exported from Benin, Ghana, and Togo, 2012–2016, shown as a proportion of total reported exports (based on exporter-reported quantities) from each country, including all countries responsible for importing 3% or more of total exports from at least one exporting country. US = USA, GH = Ghana, ES = Spain, JP = Japan, GB = UK, CA = Canada, HK = Hong Kong, TW = Taiwan, FR = France, IT = Italy. Note that for Ghana data are missing for 2016. Source: CITES trade database (http://trade.cites.org/).

For three of the main importers (the USA, the EU combined as a region, representing mainly Spain, UK, France and Italy, and Hong Kong), broad trends in the number of ball pythons imported over time suggest that whilst the role of the USA and the EU as importers declined over recent years, the role of Hong Kong as a major importer (supplied by Ghana, Togo and the USA) increased (Suppl. material 3). In parallel, the role of the USA as an exporter increased, and the USA is now the fourth largest global exporter of ball pythons responsible for the supply of ball pythons to a range of countries on all continents, including the UK, Germany, Japan, Hong Kong, Canada and Mexico (Suppl. material 3). The source of ball pythons exported from the USA shows a switch first from wild-sourced to ranched (as indicated by export source above), and then from ranched to captive-bred individuals, thus demonstrating a shift from the USA operating as a re-exporter of ball pythons documented as ranched in range states to an exporter of their own in-country production (in addition to the supply of their own [unquantified] domestic market, Suppl. material 3). Germany now also exports up to 1,600 captive-bred ball pythons each year, and is the largest exporter after range states, the USA and Canada.

Quotas and CITES Compliance

There was no statistically significant difference among the three countries in their tendency to exceed export quotas (the number of years in which quotas were exceeded) over the 21 years included in the study for either ranched (number of years quotas exceeded = 1–8; χ² = 4.05, df = 2, p = 0.132) or wild ball pythons (number of years quotas exceeded = 8–10; χ² = 0.96, df = 2, p = 618; based on importer-reported quantities; Fig. 3). But the extent to which they exceeded quotas (the number of individuals in excess of specified quotas) was statistically significantly higher for Ghana, for ranched ball pythons, than Benin (ANOVA: F_{2, 59} = 7.33, p = 0.001, post-hoc pairwise test p < 0.001), and was statistically significantly higher for Togo, for wild-sourced pythons, than Ghana (although, for the latter, the country-wide comparison was not statistically significant [ANOVA: F_{2, 57} = 2.98, p = 0.059, post hoc pairwise test p = 0.047; based on importer-reported quantities; Fig. 3]). However, national export quotas communicated to CITES, and the rate and direction of quota adjustment over time, differed among countries. For example, the annual export quota in Ghana for ranched ball pythons was initially very low (28,500) and exports that were substantially higher than agreed quotas tended to occur during the period when the quota was low (Fig. 3b). During this period (in the early 2000s), the absolute volumes of live ball python exports from Benin and Ghana were not substantially different but the export quota in Benin for ranched ball pythons was considerably higher (139,000, Fig. 3a). Ghana has since steadily increased its quota to 60,000 (Fig. 3b) whilst Benin has reduced its quota (Fig. 3a). Similarly, annual export quotas for wild specimens in Togo were exceeded on ten different occasions by up to 39,644 individuals (average 13,730) but Togo’s quotas for wild-sourced pythons were the lowest of all three countries (1,500; Fig. 3c). Post-2003, wild caught quotas were exceeded rarely in any of the three countries, and by relatively small amounts (Suppl. material 1). In Ghana, animals declared to be captive-bred were exported in excess of quotas (200 individuals, established in 2009) in three of the last five years (2012–2016; Suppl. material 1). There is no quota in Togo for ball pythons born in captivity (source code F).

Trade links

Figure 5 summarises recent (2012–2016) ball python trade links among the three main range states of Benin, Ghana, and Togo. Most notable is the role of Ghana, that appears to operate as a trade hub, re-exporting ball pythons imported from Benin and Togo. Between 2012 and 2016, 6.4% of Benin’s and 2.1% of Togo’s exports were shipped to Ghana, most (>98%) were reported as ranched (although Ghana reported a proportion exported from Togo under source code F [born in captivity]), and most (c.90%) were then re-exported by Ghana to destinations outside Africa (Fig. 5). Since 2002 (and the broad-scale introduction of the ranching source code for ball pythons), 17% of ball pythons (n = 169,610, or 210–33,873 per year) exported from Ghana were reported to have originated from Benin, and 1.9% (n = 18,790, or 220–7,340 per year) from Togo. Reciprocal ball python trade from Ghana to Benin or Togo, and trade between Togo and Benin, was reported less frequently, inconsistently, and tended to involve smaller volumes. For example, Ghana reported the export of <1,000 (predominantly ranched) ball pythons to Benin since 2002 (800 between 2012 and 2016) but these were not reported as imports by Benin. In the year 2002, 2,000 ranched ball pythons exported by Benin were reported to have originated from Togo, but there were no recorded ball python exports from Togo to Benin. Similarly, 148 ranched ball pythons exported by Togo in 1981 (n = 70) and 2004 (n = 78) were reported to have originated from Ghana but there were no matching export/import records.

Figure 5.

Exports to and from range states, 2012–2016 (including Chad which is a regional country but not listed on the IUCN Red List as a range state for ball pythons). Arrows show direction of export/import and are proportional to numbers exported. Note that 2016 figures were not available for Ghana. RoW = ‘Rest of World’. Data source: CITES Trade Database (http://trade.cites.org), based on all live ball python trade records involving range states.

Other range states were represented (as animal origin or importers) in CITES trade records to a lesser extent, and the countries involved changed over time. In the 1990s, a proportion of ball pythons exported from Benin were reported to have originated from Burkina Faso (n = 2,987), Guinea (n = 2,200) and Mali (n = 2,850), c. 3,000 wild ball pythons exported by Togo were also reported to have originated from Mali, as did 440 exported by Ghana. More recently, in 2017, 75 ranched ball pythons exported by Togo reportedly originated from Senegal, and, in 2013, 4,000 ball pythons (also ranched) originated from Chad (although the latter is a regional country and not listed on the IUCN Red List as a range state per se). There were no export records for ball pythons from either Senegal or Chad to Togo. Togo also reportedly exported c. 800 ball pythons to Niger.

Despite the relatively extensive geographical range of ball pythons, CITES trade data show that ball python production to supply the global pet trade, from within range states, remains almost exclusively sourced from three countries in the centre of their range–Benin, Ghana, and Togo (see also Toudonou 2015). Predominantly taken directly from the wild in the 1980s and 1990s, all three countries switched to ranching as the dominant reported production method in the early 2000s (see Gorzula et al. 1997). Togo has maintained relatively high levels of ranch production in recent years, but CITES trade records suggest that Benin and Ghana have not. It is not clear whether this decline in exports, from Benin, and to a lesser extent Ghana, was a conservation strategy designed to maintain exports within agreed quotas or a consequence of declining wild ball python populations required to supply production.

A significant proportion of exports from Ghana originate from Benin and Togo, implying that Ghana operates as a re-exporter (see also Pernetta 2009) in addition to a harvester of its own resources. Ghana also supplies a slightly different and more diverse market than Togo and Benin (Fig. 4), relying more on the Asian than the USA market, and exports more reportedly captive-bred specimens (Suppl. material 1). Africa exports over 100 live reptile species to Asia (notably, in addition to ball pythons, leopard tortoises Stigmochelys pardalis), and whilst exports along this trade route have increased in recent years, there has also been an increase in reports of captive-bred specimens of a number of species (Outhwaite and Brown 2018). In Benin, production in recent years has been half to a third that of Ghana and Togo (Fig. 5) and management authorities of Benin have further reduced quotas of ranched specimens to 22,000 in 2018 (UNEP 2019), perhaps in response to reports from hunters and farmers that ball pythons in Benin have declined in number and may be extirpated in some areas (see Toudonou 2015). Export quotas for ranched individuals in Togo and Ghana (as of 2019) remain at 62,500 and 60,000 (UNEP 2019), respectively. However, in recent years Ghana has exported far fewer snakes than its quota allowed (Fig. 3), whilst Togo, despite being the smallest of the three countries, largely fulfils its quota (which may, in part, be supported by informal cross border trade at the local level, D’Cruze et al. 2020b, below).

At a range-wide level, differences in the use of source codes among exporting range states, and inconsistencies in reporting of trade among range states, as well as inconsistencies in the use of source codes between exporting and importing countries, may suggest irregular trading and/or improper ranching procedures, creates confusion in monitoring ball python trade, and represents an area of potential concern (CITES AC28 Com. 5). Since 2014, a proportion of ball python exports from Togo have been declared (by Togo, and by importing countries) as source code F (born in captivity, Fig. 3) rather than R (ranched). The CITES definition for animals “born in captivity” (see Lyons et al. 2017) may be a more appropriate descriptor of individual pythons from eggs of gravid females brought in to farms during what is otherwise described as “ranching” (see D’Cruze et al. 2020b); however, hunters in Togo sell eggs and snakes to farms in Benin and Ghana (D’Cruze et al. 2020b) but neither of these countries uses the source code F in their export reports to CITES (nor do countries importing from Benin or Ghana). Whilst it is possible that the source code F is being used in Togo, for example, by new staff, or under new guidance, that has not yet been adopted elsewhere, it is also possible that since there is no quota for ball pythons born in captivity it provides a useful loophole (i.e. classifying a proportion of exports as “F” may be a mechanism to maintain export volumes of ranched specimens within agreed quotas, see Fig. 3).

A brief review of the legislation in each of Benin, Ghana and Togo highlights some contradictory text regarding the legality of the practice of ranching in these countries. In Benin, for example, a license is required by Law No. 2002–16 (2004) for the harvest, market or export of “partially protected species” (which includes ball pythons), whether for personal or commercial purposes. Collection of the eggs of partially protected species is also permitted on a limited basis but, under Article 154, it is an offence to hunt gravid females or juveniles. Since females and their juveniles of partially protected species are stated to be treated as fully protected species (Article 33), Article 36 also suggests that these animals should not be kept (except under exceptional cases for scientific purposes).

In Ghana, ball pythons are partially protected under Schedule II of the Wildlife Conservation Regulations of 1971 that prohibit hunting, capturing or destroying any species listed in Schedule II between August 1 and December 1 of each year, and hunting, capturing or destroying juveniles, or adults accompanied by juveniles, at all times. Outside of these restrictions ball pythons may be captured with possession of a valid licence according to Article 6 of the 1971 Regulations.

In Togo hunting permits are required by Articles 78, 79, 80 and 81 of Law No. 2008–09 of the Carrying Forest Code (2008) but discussions with hunters (D’Cruze et al. 2020b) suggest that not all hunters have them. Furthermore, as in Benin, it is unclear whether (even in the possession of a permit) the hunting of gravid females, juveniles, eggs and the associated destruction of ball pythons burrows (as described in D’Cruze et al. 2020b) can be carried out legally given that this activity is strictly forbidden under Article 78 of the Carrying Forest Code (2008). In Togo, sustainable management (see below) is required under Article 61 of the 005 Framework Law on the Environment (2008).

At an international level, analysis of CITES trade records of ball pythons exported from range states reveals cases of missing data (e.g., missing export records for Benin, Fig. 2), potential mis-reporting (e.g., under-reporting of annual exports by Togo) and frequent exceeding of nationally established export quotas (Fig. 3, Suppl. material 1). In addition, there is evidence that snakes exported from a particular country were in fact sourced from neighbouring range states without adequare documentation (D’Cruze et al. 2020b) potentially negating conservation measures taken within other countries.

Discrepancies between export and import data in the CITES trade database are common (e.g., Phelps et al. 2010) and may arise for a number of legitimate reasons (e.g., specimens leaving a country at the end of one year, and arriving at their destination at the beginning of the following year, in which case the same shipment is recorded at export and import under different years, UNEP-WCMC 2013) – they may also reveal irregularities and deliberate under-reporting but these are not possible to distinguish from genuine reporting errors. Over-reporting by exporters can arise when the exporting country reports the number of specimens permitted for export rather than the actual number of specimens exported (UNEP-WCMC 2013).

All three countries exceeded quotas for both ranched and wild-sourced exports in at least one year, but vast differences in quotas mean that the implications of doing so differ. Exceeding a very low, conservatively established, quota, for example, may represent a lower risk in terms of potential over-exploitation than trading within the limits of a very high quota.

Although some trade is formally documented between these three range states it is not clear to what extent CITES-recorded trade is representative of the actual inter-state trade that occurs in this region. For example, whilst Ghanaian exports include a proportion that originates from other range states there are discrepancies in the numbers traded between Benin and Ghana, and in source codes between Togo and Ghana, meaning that total regional exports (and their origins) are difficult to reliably quantify, and compliance with CITES trade quotas difficult to assess. For example, in 2012, Benin reports exporting 2,950 ball pythons to Ghana, whereas Ghana reports importing 10,500 Ball pythons from Benin–there are no transactions in either previous or later years that appear to account for the difference of almost 7,000 ball pythons.

Similarly, in 2014, Togo reported exporting 2,500 ranched ball pythons to Ghana but whilst Ghana reports importing 2,200 ranched ball pythons from Togo the following year (which may or may not be the same snakes) they also report importing 500 ball pythons born in captivity and 50 wild-sourced ball pythons in 2014 that do not appear in Togo’s export records. The involvement of other range states, albeit at a relatively lesser level, and changes in the states involved over time, suggests that, as has been observed for other species in trade (e.g., pangolins, Heinrich et al. 2016), this regional network is dynamic and may be subject to change in response to relative abundance of snakes across their range, and economic interests of neighbouring states.

That ball python hunters also hunt in neighbouring countries, and sell pythons caught in one country to snake farms in another (D’Cruze et al. 2020b) introduces further complications. In reality CITES-reported exports from Benin, Ghana and Togo are composed to at least some degree of snakes sourced informally (or illegally) from neighbouring countries (see also Gorzula et al. 1997; Owusu-Nsiah 1999).

Sustainability is difficult to assess in the absence of wild population data. Although harvest size is often monitored in lieu of wild population size, harvest may be influenced by effort (hunting period, numbers of hunters, and area hunted) and the methods used, all of which may vary over time (Weinbaum et al. 2013 and references therein). Thus, whilst, for example, declining exports from Benin may indicate declining wild populations, it could also indicate shifting focus of local income opportunities, and it does not necessarily follow that relatively stable exports from Togo indicate stable wild populations. There are no accurate wild population data available (i.e. based on robust density estimates) for this species in any part of their range (Auliya and Schmitz 2010) but 75% of Togolese hunters surveyed by D’Cruze et al. (2020b) reported that there were fewer snakes than there were five years previously, and several commented that they had to travel further to find them.

Ball python exports from all three countries are dominated by a small number of export companies (although it is possible that there are more that export exclusively to parts of the world other than the USA), and the number of companies operating in Benin and Ghana appears to have declined (although it is not possible to distinguish between a decline in the number of companies and a decline in the number of companies exporting to the USA). Further, shifting global trends (in market demand, Suppl. material 2) and increasing competition from captive-bred sources from the USA (e.g. Herrel and van der Meijden 2014) and some European countries, suggests that trade in individuals sourced directly from range states may itself not be sustainable in the long-term at present quantities.

The wider aspects of this trade: for example, risks of genetic pollution and/or disease introduction associated with improper re-release of snakes from ranches, and concerns regarding poor animal welfare at farms and in temporary holding facilities, together with documented additional uses in traditional medicine and bushmeat are discussed elsewhere (see Auliya et al. 2020, D’Cruze et al. 2020c, d, e). All such issues are potentially accentuated in a system whereby snakes are hunted and traded in convoluted trade chains throughout the region as described here (based on CITES trade patterns), and in D’Cruze et al. (2020b) (based on hunter questionnaires).