Review Article |
Corresponding author: Neil D'Cruze ( neildcruze@worldanimalprotection.org ) Academic editor: Enrico Di Minin
© 2020 Neil D'Cruze, Lauren A. Harrington, Délagnon Assou, Jennah Green, David W. Macdonald, Delphine Ronfot, Gabriel Hoinsoudé Segniagbeto, Mark Auliya.
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:
D'Cruze N, Harrington LA, Assou D, Green J, Macdonald DW, Ronfot D, Hoinsoudé Segniagbeto G, Auliya M (2020) Betting the farm: A review of Ball Python and other reptile trade from Togo, West Africa. Nature Conservation 40: 65-91. https://doi.org/10.3897/natureconservation.40.48046
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Our review of the CITES trade database confirmed that the ball python is the most exported species by Togo; with 1,657,814 live individuals – comprising 60% of all live reptiles – reported by importing countries since 1978 (almost 55,000 annually since 1992). In total, 99% of the ball pythons legally exported from Togo under CITES were intended for commercial use, presumably as exotic pets. Since the turn of the century, wild-sourced snakes exported from Togo have been largely replaced with ranched snakes, to the extent that in the last 10 years 95% of these live exports were recorded using CITES source code “R” with the majority destined for the USA. We found discrepancies in the CITES trade database that suggest ball python exports were consistently underestimated by Togo and that both ranched and wild-sourced ball python annual quotas have been exceeded on multiple occasions including as recently as 2017. Furthermore, our field visits to seven of these “python farms” revealed that they are also involved in the commercial trade in at least 46 other reptile species, including eight that are already involved in formal CITES trade reviews due to concerns regarding their sustainability and legality. Ranching operations in West Africa were once thought to provide a degree of protection for the ball python; however, in light of recent research, there is growing concern that ranching may not confer any significant net conservation benefits. Further scrutiny and research are required to ensure the long-term survival of wild ball python and other reptile species populations in Togo.
CITES, conservation, Python regius, ranching, wildlife trade
The exotic pet trade is an enormous global enterprise (
To assess the long-term sustainability of such trades, an understanding of trade patterns is crucial. With this remit, trade in ball pythons (Python regius) (a popular pet in many countries, particularly the USA), exported by Togo (one of the species’ Range States, and one of the main source countries involved in international export), is an informative case study – in part because it illustrates an almost complete shift from wild-captured individuals to the use of ranching. Ranching (defined below) is a production system, intended as a potential solution to the unsustainable harvest of wild animals, dependent on “farms” that do not function as farms in the traditional agricultural sense, rather they are continually dependent on a wild source that is by definition “surplus” to the wild population [i.e. that portion of the population that would likely suffer naturally high mortality rates in the wild (CITES glossary 2019, https://www.cites.org/eng/resources/terms/glossary.php)]. This paper explores changing trade patterns (numbers, source, and markets) in ball pythons from Togo, carried out as part of a broader study of the relationships between in-situ and ex-situ harvesting with respect to sustainable wildlife use. Here we focus on the farms involved in ball python trade (the extent and changing nature of their trade, including the markets that they supply, and other reptiles collected for export), elsewhere we address ball python supply (
Togo is a relatively small West African country (56,790 km2) bordered by Ghana to the west, Benin to the east, Burkina Faso to the north and the Gulf of Guinea to the south. It comprises a long strip of land located between a latitude of 6°–11°N and a longitude of 0°–2°E, stretches over 660 km from north to south and has a coastline of 50 km, east-west (
Research focused on reptile diversity in Togo date back to the time of German colonisation and herpetologists such as Sternfeld who published the first inventory of Togolese snakes that included a total of 75 species (
Togo is recognised to be one of the main reptile exporters of sub-Saharan western Africa with several species currently harvested at significant levels for the international “exotic” pet trade (
Much of the international ball python trade can be traced back to a number of registered reptile “farms” that are in operation across West Africa, most notably Benin, Ghana and Togo (
In terms of international trade regulation, the family Boidae (including all species taxonomically assigned to the Pythonidae) has been listed on the Appendices of CITES since 1977 (except Boa constrictor that was listed in 1975). Togo joined CITES in 1978, and entered into force in 1979 (
Despite the relatively long-standing history of ball python ranching in Togo and recent / on-going endorsement from major importers such as the EU, the last detailed examination of ball python production systems in West Africa was carried out almost 15 years ago (
(1) Assess the extent and characteristics (source, purpose and destination) of ball python trade originating from Togo.
(2) Quantify changes over time in the Togolese ball python trade, specifically with respect to the role of ranching and conformity with national annual trade quotas.
(3) Provide a preliminary assessment of the wider activities of reptile farms in Togo with respect to the other species involved.
The overall objective of this study was to gain insights into potential impacts that this type of wildlife trade activity has on ball pythons and other reptiles in Togo. Ultimately, we hope our findings, and other recently published research focused on the reptile trade in Togo, will inform future interventions to aid conservation initiatives for this important site of herpetological biodiversity.
To determine the number of ball pythons exported from Togo, trade data were obtained from the CITES database. Countries exporting or importing species recognised by CITES are responsible for recording each trade transaction; a central database of all trade is publicly available at https://trade.cites.org/. To obtain numbers of ball pythons traded from Togo, all trade records pertaining to ball pythons exported from Togo, for all purposes, all source codes (outlined in Notification 2002/022) and all trade terms, were downloaded as a comparative tabulation from the CITES trade database. Further analysis of the trade data was limited to records of exports reported as “live” and for “Commercial” (T), “Breeding” (B), “Zoological” (Z) or “Personal” (P) use. All importing countries were included in the search criteria. Trade between the years 1978 (the year that Togo joined CITES) and 2018 were considered, and both exporter- and importer-reported quantities were used, and compared. Each “live animal” reported was presumed to represent an individual animal. The same data were obtained from the CITES trade database for all reptiles exported from Togo to enable assessment of the relative importance of ball pythons in the Togolese reptile trade.
Information detailing the annual trade quotas implemented by Togo (1997–2017) was obtained from the Species+ website (
For the USA specifically, the number of ball pythons imported from Togo between the years 2000 and 2017, was 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 which was received on 08.05.18 (control number FWS-2018-00788). This provided an independent source of trade data for one of the main importing countries for ball pythons, as well as additional information on individual Togolese exporters.
Research teams (composed of five different individuals) visited and collected data from eight different reptile farms across Togo during three field trips in 2018 (February, June and October) and two field trips in 2019 (February and April) lasting on average between 10 and 21 days. All official visits were organised under the guidance and permission of the CITES Scientific and Management Authorities in Togo. Photos of reptile species observed were taken with the consent of the farm owners; however, our aim was not to carry out a full inventory of the farm owner’s stock. Rather, the images were taken to aid subsequent taxonomic identification. For all species, binomial nomenclature and information regarding their conservation, population status, and distribution was gathered from the IUCN Red List of Threatened species (hereafter the IUCN Red List,
To test for trends over time in ball python exports from Togo, as recorded in CITES trade records, we summarised the records by year and used the tslm function in the “forecast” package (
The CITES trade database (https://trade.cites.org) contained 4,863 records of (live and dead) reptile exports from Togo between 1978 and 2017 (i.e. exports under all trade terms, including live animals, bodies and body parts), involving at least 51 species of 28 genera. 15% (n = 723) of all reptile trade records involved ball pythons, and 98% (n = 710) of those involved live snakes. Overall, 94% [n = 4,564] of all reptile trade records involved live animals. In total, ball python trade records, documenting exports from Togo between 1978 and 2017, represented the export of between 963,344 and 1,657,814 live individuals (according to exporter- and importer-reported quantities, respectively) – these figures comprised 53% of all live reptiles reported by Togo as exports during this period (Fig.
The proportion of all reptile species reported as live exports by Togo (1978–2017) in each taxonomic order and family. Source: CITES trade database, https://trade.cites.org
According to both exporter- and importer-reported quantities, live ball python exports from Togo increased from < 14,000 per year in the late 1970s/early 1980s [following which there was a statistically significant increase of one to two thousand per year (1978 – 1987: exporter-reported trend = 1,974 per year, F1, 8 = 35.8, P < 0.001, R2 = 0.82; importer-reported trend = 1,490 per year, F1, 8 = 50.6, P < 0.001, R2 = 0.86)] to approximately 60,000 in 1991 (a four-fold increase over the 4 years between 1988 and 1991), reaching a peak of 74,751 (as reported by importing countries) in 1994 (Fig.
A Number of individual live ball pythons exported from Togo as reported by CITES, 1978- 2017, showing exporter- (red) and importer-reported (blue) quantities against timeline of events associated with the regulation of ball python trade. Note that exporter-reported quantities were not available for 2017 at the time of analysis. B Annual discrepancies between exporter- (Togo) and importer-reported quantities. Source: CITES trade database, https://trade.cites.org
Discrepancies between annual exporter- and importer-reported quantities (Fig.
In total, and according to both exporter- and importer-reported quantities, 99% (n = 950,829 and 1,647,639 respectively) of individual live ball pythons exported from Togo were intended for commercial use (presumably as exotic pets). Since the years 1999/2000 wild-sourced snakes exported from Togo were largely replaced with ranched snakes (Fig.
Reported source of ball pythons exported from Togo, based on importer-reported quantities obtained from CITES trade records. Note that the CITES trade database does not contain source information for most records prior to 1991 (unless the specimen was specifically declared as captive-bred,
CITES trade records reported exports of ball pythons from Togo to 58 different countries between 1978 and 2017, in total quantities for the period that varied between 1 and over 1 million ball pythons per country; note, however, that minima and maxima represent extreme cases, and that, for most (71.4%) countries, reported exports ranged between 100 and 9,000 ball pythons. Both exporter- and importer-reported quantities showed the USA to be the largest importer, responsible for between 60 and 77% of exports (for exporter- and importer-reported quantities respectively). Six other countries reported importing >1% of the total over this period: France (7.5%), Germany (4.3%), Italy (2.7%), Spain (1.3%), Belgium (1.2%), and Japan (1.1%). Exporter-reported quantities suggested that three additional countries – the Netherlands, Hong Kong and Ghana – also imported >1% of the total (1.6, 1.3 and 1.7, respectively). At a regional level, Europe was second to North America (USA and Canada; there were no exports reported to Mexico) as importer of Togolese ball pythons, responsible for between 30 and 20% of exports (for exporter- and importer-reported quantities respectively) (Fig.
The annual number (A) and proportion (B) of ball pythons from Togo imported by three main world regions (Asia, Europe and North America), 1978–2017. Proportion shown as % total ball python imports from Togo. Data derived from Togo export records on CITES trade database, and based on importer-reported quantities. Source: CITES trade database, https://trade.cites.org
Since the 1990s (following an increase in ball python exports from Togo in the latter half of the 1980s; see Fig.
In the 21 years between 1997 and 2017, importer-reported quantities suggest that ranched ball python annual quotas have been exceeded on six different occasions (by an average of 10,421, maximum 19,787), most recently in 2013 (by 12,626 ball pythons, Fig.
The number of ranched (A) and wild (B) specimens of ball pythons exported annually since 1997, according to export data (from Togo) and import data (from all importing countries) recorded on CITES trade database, in comparison with the annual quota set for ball python exports from Togo. Source: CITES trade database, https://trade.cites.org
The LEMIS trade database documents the import of a total of 764,527 live ball pythons from Togo into the USA since the year 2000. Ball pythons came from 11 independent Togolese exporters, two of which (Togamin and Pajar Sarl) were responsible for 88% of all ball pythons imported over this period (55%; n = 422,867 and 33%; n = 251,969, respectively, Fig.
The number of ball pythons exported by the different reptile farms in Togo into the USA annually since 2000, as recorded on LEMIS trade database, shown against CITES-reported USA imports (Source: CITES trade database, https://trade.cites.org).
In total, (including only those identified to species level, plus those of ambiguous taxonomic status indicated by “cf.”) 46 reptile species were observed during visits to the eight different farms in Togo (including seven python farms and one venom farm) between February 2018 and April 2019, including 1 Crocodylia (2%), 10 Sauria (21%;), 24 Serpentes (52%;), and 11 Testudines (24%) (please see Appendix
With regards to conservation and population status of the 46 species observed, over half (59%, n = 27) had not yet been evaluated on the IUCN Red List. Of the 19 observed species that were included on the IUCN Red List most (68%, n = 13) were categorised as Least Concern but for most of these (n = 12, 63% of all Red List species) conservation status was unknown (please see Appendix
With regards to the geographic distribution of these 46 species, a total of 10 species (22%) are considered as regionally endemic to West Africa, and 32 species (70%) are considered as widespread (extending to regions outside western Africa) according to information provided by the IUCN Red List (
Togo remains a substantial source of live reptiles, both native and non-native, with at least 19 CITES-listed species currently held at reptile farms. In terms of the number of animals traded, the most notable species exported by Togo since 1978 under CITES is the ball python; with 1,657,814 live individuals - comprising 60% of all live reptiles – reported by importing countries. In total, 99% of the ball pythons legally exported from Togo under CITES have been intended for commercial use as exotic pets. Since the turn of the century, wild-sourced snakes exported from Togo have been largely replaced with specimens declared as “ranched (R)”, to the extent that in the last 10 years 95% of all live exports were recorded using CITES source code “R”. Ball pythons have been exported from Togo to 58 different countries since 1978. With regards to the global trade trend, CITES importer-reported quantities suggest that numbers of ball pythons exported from Togo since 1992 until 2019 (following a rapid increase in reported trade levels in the late 1980s/early 1990s) have overall remained relatively stable (at an annual average of 54,754 live animals), albeit with considerable fluctuation among years (Fig.
The provision of captive breeding and ranching operations as a replacement for the potentially unsustainable sourcing of wildlife from their natural habitats, as observed for ball python CITES exports reported from Togo, is not new (e.g.,
In the context of ball pythons, recent scientific studies have raised conservation concerns regarding current production methods being implemented in West Africa to supply the international exotic pet trade. In Benin,
The ball python has a relatively large distribution, fast reproductive rate, and occurs in a wide range of habitats including some areas with formal protected status and some areas inhabited by local communities who consider the species to be sacred (
Animal welfare impacts are associated with every step of a wildlife trade chain including capture, restraint, transport and subsequent captivity irrespective of a species’ legal status, but they rarely feature in the relevant published scientific literature (
Images of species encountered during visits to the eight snake farms: A juvenile Python regius B example housing conditions C juvenile Varanus ornatus; and D juvenile Varanus exanthematicus. Images show typical barren enclosures with overt overcrowding, no shelter and species exhibiting interactions with transparent boundaries. Photos: A, B (Neil D’Cruze) C, D (M. Auliya).
Our study provides the most complete account of species diversity present at snake breeding farms in Togo that has been published to date. Many of these species, like ball pythons, are not currently considered threatened according to the IUCN Red List assessment, but although there was no evidence that farms were specifically selecting threatened species, they were not avoiding them either. And, for species that have been categorised as non-threatened, trade is being carried out in a manner that means that a non-threatened status is not necessarily still the case or will be in future. This is reflected by the fact that a number of species observed during our visits to ball python breeding farms are already currently involved in the CITES Review of Significant Trade, a procedure [defined in Res. Conf. 12.8 (Rev. CoP18)] designed to identify species that may be subject to unsustainable levels of international trade, and to identify problems and solutions concerning effective implementation of the Convention (
Similarly, a number of species observed during our visits to ball python farms are already currently involved in the CITES Review of Trade in Animal Specimens Reported as Produced in Captivity, a procedure (defined in Resolution Conf. 17.7 and Decision 17.105) designed to help prevent the inadvertent misuse of CITES source codes, and deliberate fraudulent claims that wild-caught specimens were captive bred. Specifically, Varanus exanthematicus and Centrochelys sulcata from Togo have been included in this process due to recent high volumes of trade, shifts, and international concerns that these species are not being “ranched” in conformity with CITES requirements [as stated in Res. Conf.11.16 (Rev. CoP15)]. In the case of C. sulcata there are also specific concerns regarding the questionable use of source code “F” (born in captivity) and “R” (ranched) given that this species is not native to Togo.
Our field visits now draw attention to a longer list of species for potential consideration in future CITES review procedures. Togo has a well-established infrastructure for intercontinental shipments and has been identified as one of the major hubs for the export of live African reptiles (
CITES trade records are known to be incomplete and error-prone (e.g.,
Our time at the eight snake facilities in Togo was limited and intermittent. It is therefore very likely that species lists compiled are incomplete and thus should be treated as an initial conservative list only. The assumption, that these species lists are incomplete, is also supported by species groups such as the Egyptian cobra (Naja haje) (
In light of recent concerns regarding the hunting and release practices that underpin python farms in West Africa (Toudonou, 2015;
The aim of this paper was to provide information specific to the ball python trade in Togo to inform current management practice. Additional information is needed – notably, on the understanding, attitudes and behaviour of consumers, as well as on the population dynamics and status of ball pythons. More broadly, this system is of interest to those concerned with sustainable use, substitutability, and the links between the various forms of “captive” and wild populations, and as such has parallels with a number of other traded wildlife species including ranched crocodilians (
Legal and sustainably managed commercial wildlife trade has been proposed as a vital conservation tool, that in some cases is necessary to ensure the long-term survival of wild populations (
The ball python is the most commercially traded live wild animal under CITES from Africa over the past five years which have ostensibly involved ranching operations (
We wish to thank the CITES Management Authorities of Togo (especially Mr Apla Yao Mawouéna and Mr. Okoumassou Kotchikpa) who facilitated access to reptile breeding farms. Thanks especially to Kinam Kombiagnou (Directeur de l’élevage, Ministère de l’ agriculture, de l’élevage et de la pêche) for issuing relevant permit. We further thank all farm owners (especially Mr. Koudeha, Emmanuel and Mrs Sambo) who accepted the examination of the specimens and the sampling of buccal swabs. Further, the help of local guides was indispensable during field work. Thanks also to Peter Paul van Dijk for useful comments. Finally, we sincerely thank Agbo-Zegue NGO for providing logistics.
Reptile species observed across seven reptile farms in Togo (2018–2019), with associated IUCN Red List and CITES Appendices classifications. “Distribution” refers to the geographical distribution of the species and allocated to: “RE” = Restricted to western Africa i.e. Benin, Burkina Faso, Cape Verde, The Gambia, Ghana, Guinea, Guinea-Bissau, Ivory Coast, Liberia, Mali, Mauritania, the Niger, Nigeria, Senegal, Sierra Leone and Togo); “W” = widespread species also occurring in Africa outside of this region; when “RE” or either “W” are attached with a “1” means that the species is native to Togo; when “RE” is attached with a “2” implies that western African species extend beyond this region, and when “W” or either “RE” is attached with a “3” that the species is definitely, or likely also supplied by another country or range State; exotic species not distributed on the African continent were classified with “Other”; *): resurrected from Crocodylus niloticus (
Family | Species | IUCN Conservation Status | Date Assessed (IUCN) | Population Status (IUCN) | CITES Status | Distribution Status |
---|---|---|---|---|---|---|
Crocodylidae | Crocodylus suchus* | NE | NA | I | RE2,3 | |
Agamidae | Agama agama | NE | NE | NL | W1 | |
Agamidae | Agama sp. | NA | NA | NA | NA | |
Agamidae | Uromastyx geyri | NT | July 2012 | Decreasing | II | RE3 |
Agamidae | Uromastyx sp. | NA | NA | NA | NA | |
Chamaeleonidae | Chamaeleo senegalensis | VU | July 2012 | Unknown | II | RE1 |
Eublepharidae | Hemitheconyx caudicinctus | LC | July 2012 | Unknown | NL | RE2,3 |
Gerrhosauridae | Broadleysaurus major | NE | NE | NL | W1, 3 | |
Scincidae | Mochlus fernandi | NE | NE | NL | W1,3 | |
Scincidae | Scincopus fasciatus | DD | June 2009 | Unknown | NL | W3 |
Varanidae | Varanus exanthematicus | LC | June 2009 | Unknown | II | W1,3 |
Varanidae | Varanus niloticus | NE | NE | II | W1 | |
Varanidae | Varanus ornatus | NE | NE | II | RE2,3 | |
Boidae | Calabaria reinhardtii | NE | NE | II | W1,3 | |
Boidae | Eryx muelleri | NE | NE | II | W1,3 | |
Colubridae | Dasypeltis cf. gansi | NE | NE | NL | W1 | |
Colubridae | Dasypeltis sp. | NA | NA | NA | NA | |
Colubridae | Dasypeltis confusa | NE | NE | NL | W1 | |
Colubridae | Dispholidus typus | NE | NE | NL | W1 | |
Colubridae | Philothamnus cf. irregularis | LC | June 2009 | Unknown | NL | W1 |
Elapidae | Dendroaspis angusticeps | NE | NE | NL | W | |
Elapidae | Dendroaspis jamesoni | NE | NE | NL | W1,3 | |
Elapidae | Dendroaspis polylepis | LC | June 2009 | Stable | NL | W3 |
Elapidae | Dendroaspis viridis | LC | July 2012 | Stable | NL | W1, 3 |
Elapidae | Naja melanoleuca** | NE | NE | NL | W1 | |
Elapidae | Naja nigricollis | NE | NE | NL | W1 | |
Elapidae | Naja sp. | NA | NA | NA | NA | |
Lamprophiidae | Mehelya poensis | NE | NE | NL | W1 | |
Psammophiidae | Psammophis cf. sibilans | NE | NE | NL | W1 | |
Psammophiidae | Rhamphiophis oxyrhynchus | NE | NE | NL | W1 | |
Pythonidae | Morelia viridis | LC | June 2017 | Stable | II | other |
Pythonidae | Python regius | LC | June 2009 | Unknown | II | W1,3 |
Pythonidae | Python sebae | NE | NE | II | W1 | |
Viperidae | Atheris chloroechis | LC | July 2012 | Unknown | NL | RE1 |
Viperidae | Bitis arietans | NE | NE | NL | W1 | |
Viperidae | Bitis gabonica | NE | NE | NL | W3 | |
Viperidae | Bitis nasicornis | NE | Unknown | NL | W1, 3 | |
Viperidae | Echis ocellatus | NE | NE | NL | W1 | |
Viperidae | Echis pyramidum | LC | June 2009 | Unknown | NL | RE3 |
Viperidae | Echis sp. | NA | NA | NA | NA | |
Pelomedusidae | Pelomedusa subrufa** | NE | NE | NL | W1,3 | |
Pelomedusidae | Pelusios c. castaneus | NE | NE | NL | RE1,3 | |
Pelomedusidae | Pelusios niger | NT | May 2018 | Decreasing | NL | RE1,3 |
Testudinidae | Centrochelys sulcata | VU | Aug 96 | Unspecified | II | W3 |
Testudinidae | Kinixys belliana | NE | Aug 96 | NE | II | W3 |
Testudinidae | Kinixys erosa | DD | Aug 96 | Unspecified | II | W1,3 |
Testudinidae | Kinixys homeana | VU | January 2006 | Decreasing | II | RE1,3 |
Testudinidae | Kinixys nogueyi | NE | NE | II | RE1,3 | |
Testudinidae | Stigmochelys pardalis | LC | Aug 14 | Unknown | II | W3 |
Trionychidae | Cyclanorbis senegalensis | VU | May 2016 | Decreasing | II | W1 |
Trionychidae | Trionyx triunguis | VU | June 2016 | Decreasing | II | W1 |
Conservation (A) and distribution (B) status of reptile species (n = 46 and n = 43, respectively) observed on Togolese farms. Conservation status as categorised by the IUCN Red List (