Research Article |
Corresponding author: Lauren A. Harrington ( lauren.harrington@zoo.ox.ac.uk ) Academic editor: Franco Andreone
© 2020 Lauren A. Harrington, Jennah Green, Patrick Muinde, David W. Macdonald, Mark Auliya, Neil D'Cruze.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Harrington LA, Green J, Muinde P, Macdonald DW, Auliya M, D'Cruze N (2020) Snakes and ladders: A review of ball python production in West Africa for the global pet market. Nature Conservation 41: 1-24. https://doi.org/10.3897/natureconservation.41.51270
|
The ball python (Python regius) is the most traded, CITES listed, live animal exported from Africa. Recent studies have raised concerns as to whether production methods in Africa are sustainable, humane and compliant with legislation. To aid future management we explored export patterns, using the CITES and U.S. LEMIS database, for live ball pythons from across their range in West Africa to identify the main exporters and the main markets supplied, and to assess associated trends, and compliance with nationally-established export quotas. We found that export to supply the global pet trade remains almost exclusively carried out by three range countries – Benin, Ghana, and Togo. The USA was the largest importer from all three countries, although Ghana appeared to be less dependent on the USA market than either Togo or Benin, exporting to a more diverse range of countries, particularly in Asia. Between 2003 and 2017 there was a decline in annual importer-reported exports from Benin and from Ghana, but not from Togo. Ghana appears to operate as a regional trade hub, re-exporting ball pythons imported from Benin and Togo, and exports more ball pythons reported as captive-bred. Trade records from all three countries exhibited a switch from predominantly wild-sourced to predominantly ranched individuals. However, 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, represent areas of potential concern. We recommend a regional-level policy approach for this highly sought-after species, to safeguard ball pythons and local livelihoods.
CITES, Python regius, ranching, reptile, wildlife trade, Benin, Ghana, Togo
International wildlife trade can only be sustainable if harvest (or offtake) at the national level is sustainable (
In this study we explore export patterns for live ball pythons (Python regius) from across their West African range, focusing specifically on captive-production systems. Ball pythons are an internationally renowned and popular pet, particularly in the USA, where they are sourced from both domestic captive breeding and international export from range countries (cf.
Native to western Africa and northern parts of central and eastern Africa, ball pythons occur in a wide range of savannah habitats, including open woodlands, rainforest margins, forest/plantation mosaics, and agricultural land, from Senegal to South Sudan and Uganda (
a Approximate distributional range of ball pythons in west and central Africa (shaded orange), showing relative export volume (number of individuals) of ball pythons exported from range states (depicted as proportionally-sized circles), 1978–2017. b Trends in annual exports for the three main exporting countries and all others combined. Species range from
Locally, in range countries, ball pythons are also taken from the wild for bushmeat, leather and use in traditional medicine (
The centre of the ball pythons’ distributional range is Ghana (238,535 km2) and Benin (112,622 km2) that frame Togo (56,790 km2) to the west and east, and in the south all three countries have a coastline to the Gulf of Guinea (Fig.
All trade records pertaining to ball pythons exported alive from range states (as listed on the IUCN Red List) were downloaded from the CITES Trade Database (https://trade.cites.org/) in September 2019. We included all importing countries and territories (as listed by CITES), and all source codes (as outlined in
Additional trade data, for the period 2000–2017, detailing individual export and import companies, were obtained from the U.S. Fish and Wildlife Service Law Enforcement Management Information System (LEMIS) via a Freedom of Information Act (FOIA) request submitted to the Fish and Wildlife Service, Office of Law Enforcement (received on 8 May 2018, control number FWS-2018-00788). This level of information was only available for ball python trade to the USA.
Finally, to provide further insight on global market trends, for those importing countries (or regions) identified as important for range country exports, we repeated the CITES data collation (in November 2019) using all live ball python trade records from all exporting countries. For all major importing countries (or regions) identified, we assessed overall import trends over time, and, for the USA, known to be a major captive producer of ball pythons (
Trade data were described using graphs and summary statistics. To test for trends over time in CITES trade records, we summarised the records by year and used the tslm function in the “forecast” package (
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.
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.
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: F2, 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.
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.
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 (
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.
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
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
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.
Trade links
Figure
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
A significant proportion of exports from Ghana originate from Benin and Togo, implying that Ghana operates as a re-exporter (see also
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.
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 (
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.
Discrepancies between export and import data in the CITES trade database are common (e.g.,
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,
That ball python hunters also hunt in neighbouring countries, and sell pythons caught in one country to snake farms in another (
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 (
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
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
A multidisciplinary review in Togo (
Previous reviews of ball python production methods in West Africa have recommended a tripartite approach between the three main ball python exporters in West Africa (Benin, Ghana, and Togo) to ensure an effective regional-level conservation management plan for this species (e.g.,
At an international level, ball pythons have been included in a number of CITES driven processes in recent years but these have not taken the regional dynamics of python production into account. Specifically, at the CITES Conference of the Parties in 2016 (CoP17) Benin was encouraged to: (1) design and implement a management program for the species; (2) make non-detriment findings based on studies of the species, basic demographics, harvest and trade in the species; and (3) strengthen national regulations relating to trade control and monitoring, including stricter control policies for production systems (Dec. 17.276). However, at Animals Committee 30 the CITES Secretariat reported that Benin had not provided this information as requested. With regards to Togo, the ball python was not included in the Review of Significant Trade at Animals Committee 29 due to the incorrect assumption that it was already included in CITES Decisions (Dec. 17.276). To date, it appears that Ghana has not been requested to provide any similar information to CITES despite its prominent role in ball python production in West Africa. Instead of extending Decision 17.276 after the CoP18 in 2019, The United Nations Environment Programme – World Conservation Monitoring Centre was instead requested to "pay particular attention to Python regius from Benin, when performing its initial analysis of trade data" (CoP 18 Doc. 25). We recommend that this request be extended to Togo and Ghana. We also reiterate the recommendation that ball pythons in Benin, Togo, and Ghana should be considered for inclusion in future CITES procedures [e.g., Reviews of Significant Trade procedures (that would specifically delve into the sourcing of ball pythons from the wild), or Trade in Animal Specimens Reported as Produced in Captivity (that would focus on other issues related to those snakes reported as ranched)] at the next Animals Committee meeting.
This regional-level analysis reveals inconsistencies in management approaches among the three countries, and raises some concern regarding the sustainability of ball python trade in this region. It is clear that robust scientific information, that is currently lacking, is needed to determine the full current impact of the large scale international commercial trade on wild ball python populations and that this needs to be translated into policy in a cohesive way, particularly at a regional level in West Africa. Our findings, together with other recent studies in Benin and Togo (Toudonou, 2015;
Thanks to Peter Paul van Dijk and Erica Lyman for useful comments on the use of CITES data. Mark Auliya and Lauren Harrington received a grant from World Animal Protection to carry out this research.
Figure S1
Data type: CITES trade data
Explanation note: Annual ball python exports from range states shown against quotas.
Figure S2
Data type: CITES trade data
Explanation note: Global maps showing destination countries for ball pythons exported from Benin, Ghana and Togo.
Main importing countries: additional data
Data type: Additonal data for main importing countries and regions
Explanation note: Annual import volume and supply countries for ball python imports to the USA, the EU and Hong Kong, and annual export volume, countries supplied and source for ball pythons exported from the USA.