UNEP-WCMC technical report

Review of Chelonoidis carbonaria from Suriname (source F)

(Version edited for public release)

2 Review of Chelonoidis carbonaria from Suriname (source F ) Prepared for The European Commission, Directorate General Environment, Directorate E - Global & Regional Challenges, LIFE ENV.E.2. – Global Sustainability, Trade & Multilateral Agreements , Brussels, Belgium

Published May 2014

Copyright European Commission 2014

Citation UNEP-WCMC. 2014. Review of Review of Chelonoidis carbonaria from Suriname (source F) . UNEP-WCMC, Cambridge.

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Contents 3

Introduction and summary ...... 4 Chelonoidis carbonaria ...... 5 References ...... 9 Appendix ...... 11

4 Introduction and summary

This report reviews the conservation status and trade levels of Chelonoidis carbonaria from Suriname, with particular focus on trade in captive-born (source F) specimens, to inform discussions by the Scientific Review Group on the sustainability of trade.

CITES Resolution Conf. 12.3 (Rev. CoP16) recommends that source code F indicates " animals born in captivity (F1 or subsequent generations) that do not fulfil the definition of ‘bred in captivity’ in Resolution Conf. 10.16 (Rev.), as well as parts and derivatives thereof " and that source code R indicates " 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 ".

Permits for both sources F and R require a non-detriment finding and there are a number of European Union decisions at the species/country level for these sources. The SRG is currently assessing these decisions. Based on information presented at the 66 th meeting of the SRG, the Chair invited Member States to provide comments on the suggested treatment of the currently valid decisions by 10 th of January 2014. The SRG subsequently decided that a number of opinions may warrant more in-depth review, with particular focus on trade in sources F and R, and the following species/country combinations were selected:

• Python regius from Togo

• Stigmochelys pardalis from Mozambique and Zambia

• Chelonoidis carbonaria from Suriname

This report presents a review of C. carbonaria and any information on captive production in Suriname.

This review and others listed above indicate that countries may not always be using the most appropriate source codes, as evidenced in trade reporting patterns and where information is available on production systems. Differences over the interpretation of source codes may, in some cases, have led to the introduction of EU trade restrictions for specimens from particular sources.

Where there are concerns that source codes may not match the production system in use, it may be appropriate to adopt a no opinion iii): Referral to the SRG (the species is not currently/only rarely in trade, but is of sufficient conservation concern that the SRG has determined that any application must be referred to the SRG for a decision before a permit is issued or refused). This would enable an exchange of information with the exporting country and identification of the appropriate source code.

Furthermore, the application of country-level opinions for sources F and R may not be straightforward where new facilities become involved in the production of specimens.

REPTILIA: TESTUDINIDAE 5 Chelonoidis carbonaria II/B

SYNONYMS : Geochelone carbonaria, Testudo boiei, Testudo carbonaria

COMMON NAMES: Red-footed tortoise (English), Tortue charbonnière (French), Tortuga de patas rojas (Spanish)

RANGE STATES: Anguilla (int.), Antigua and Barbuda (int.), Argentina, Barbados (int., ext.), Bolivia (Plurinational State of), Brazil, British Virgin Islands, Colombia, Dominica (int.), French Guiana, Grenada (int.), Guyana, Montserrat (int.), Panama, Paraguay, Saint Vincent and the Grenadines (int.), Suriname, Trinidad and Tobago, Venezuela (Bolivarian Republic of), Virgin Islands of the USA (int.)

UNDER REVIEW: Suriname

EU DECISIONS: Current no opinion iii) for wild specimens from Anguilla, Antigua and Barbuda, Barbados, Bolivia (Plurinational State of), Brazil, British Virgin Islands, Colombia, Dominica, Grenada, Montserrat, Paraguay, Saint Vincent and the Grenadines, Trinidad and Tobago, Venezuela (Bolivarian Republic of) and Virgin Islands of the USA first formed on 15/12/1997 and confirmed on 25/06/2004.

Current no opinion iii) for wild specimens from Argentina and Panama formed on 10/12/1999 and confirmed on 25/06/2004. Previous Article 4.6(b) import restriction for wild specimens from Argentina and Panama first applied on 22/12/1997 and removed on 24/09/2000.

Current no opinion ii) for wild specimens from Guyana formed on 07/02/2013 and confirmed on 28/05/2013. Previous positive opinion for wild specimens from Guyana formed on 15/12/1997 and removed on 07/02/2013.

Current positive opinion for wild specimens from Suriname formed on 15/05/2002, and positive opinion for source F specimens with < 7 cm plastron length formed on 22/02/2000. Previous no opinion iii) for wild specimens from Suriname formed on 15/12/2000 and removed on 15/05/2002.

IUCN: Not evaluated

Trade patterns 6 Suriname published export quotas for 630 Direct trade to the rest of the world 2003- live, wild-sourced Chelonoidis carbonaria 2012 comprised principally live, wild-sourced every year 2003-2014. Trade appears to have specimens and relatively low numbers of remained within the quota in every year, captive-born specimens exported for according to data reported by both the commercial purposes (Table 2). The main importers and Suriname (Table 1). importer was the United States of America.

Direct exports of C. carbonaria from The only indirect exports of C. carbonaria to Suriname to the EU-28 2003-2012 comprised the EU-28 2003-2012 originating in Suriname a moderate number of wild and captive-born consisted of 10 wild-sourced live specimens live specimens exported for commercial imported via the United States, as reported purposes (Table 2). The main importer was by importers. the Netherlands. Trade data by EU Member State is available here: https://db.tt/4S7755QS .

Table 1: CITES export quotas for live Chelonoidis carbonaria from Suriname and global direct exports, as reported by importers and exporters, 2003-2014. Virtually all trade was for commercial purposes. For each year, trade to which the quota does not apply is greyed out; in 2010-2012 the quota applied to wild-sourced specimens. (At the time of data extraction, Suriname’s annual report for 2012 had not yet been received; trade data for 2013 and 2014 are not yet available.)

Reported by 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

Quota (live) 630 630 630 630 630 630 630 630 630 630 630 630 W Importer 380 403 411 508 369 279 166 168 165 200 Exporter 427 503 429 466 419 324 506 179 324

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 16/04/2014.

Table 2: Direct exports of Chelonoidis carbonaria from Suriname to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was in live specimens. (At the time of data extraction, Suriname’s annual report for 2012 had not yet been received.)

Importer Source Purpose Reported by 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 Total

EU F T Importer 80 100 160 41 150 250 100 100 117 1098 Exporter 80 100 160 25 150 200 715 W T Importer 134 110 160 254 148 84 16 76 80 149 1211 Exporter 134 125 187 229 158 99 338 93 225 1588 RoW F T Importer 22 27 49 Exporter 16 50 54 6 126 W S Importer Exporter 1 1 T Importer 246 293 251 254 221 195 150 92 85 51 1838 Exporter 293 377 242 237 261 225 168 86 99 1988

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 16/04/2014.

Taxonomic note The species has not been assessed for the 7 Chelonoidis carbonaria was previously IUCN Red List to date. The species was included in the genus Testudo and more considered ‘not threatened globally’ in the recently, Geochelone (Fritz and Havaš, CITES Review of Significant trade in 1993 2007). Through an analysis of mitochondrial (WCMC et al. , 1993) and Bonin et al. (2006) and nuclear genes, Le et al. (2006) placed considered it to be abundant throughout its the species within the genus Chelonoidis , range and not directly threatened. However, and this was accepted in the current CITES population declines were reported in some Standard Nomenclature (Fritz and Havaš, areas (Walker, 1989; WCMC et al. , 1993), 2007). particularly affecting island populations (Kaur, 2011). Furthermore, in a more recent Conservation status draft assessment by the IUCN/SSC Tortoise C. carbonaria is a relatively large South and Freshwater Turtle Specialist Group in American tortoise that occupies a wide 2011, C. carbonaria was categorized as range of habitats, including savannas and ‘Vulnerable’, and it was noted that its wide adjacent forest areas (Vargas-Ramírez et al. , distribution was “associated with regional 2010; Walker, 1989; Ojasti, 1996), from dry variability and conservation focus of forests to rainforests (Pingleton, 2009). It different lineages”, and that there was a lack reaches sexual maturity at approximately 8- of information on population dynamics 12 years (Pingleton, 2009) and produces throughout the range (IUCN/SSC Tortoise clutches of 2-15 eggs (Kaur, 2011). Bonin et al. and Freshwater Turtle Specialist Group, (2006) reported up to four clutches per year, 2012). with around 12 eggs per clutch. In a study Bonin et al. (2006) considered habitat loss to conducted at a commercial turtle farm in be the main threat to the species. However, Venezuela, Hernández and Boede (2008) in genetic analyses conducted on Brazilian found that females were capable of populations, Farias et al. (2007) found producing a maximum of eight clutches per evidence of recent population expansion as a year. Lowman (1996; in Pingleton, 2009) result of increases in suitable habitats. reported 6-8 clutches per year of 3-6 eggs in captivity. However, Garstecki (2006) Many authors considered overhunting to be considered the species’ reproductive the main threat to C. carbonaria (Walker, potential to be low. Life spans of 56-66 years 1989; Spiess, 1997; Kaur, 2011). Spiess (1997) were recorded (Pingleton, 2009). considered C. carbonaria to be susceptible to overhunting due to its slow maturation and The range of C. carbonaria was reported to relatively low clutch size. C. carbonaria was reach from Panama, Venezuela, Colombia reported to be exploited for food throughout and the Guianas in the north to Bolivia, its range (Hernández, 1997), and Bonin et al . eastern Brazil, Paraguay (King and Burke, (2006) indicated that it was commonly 1989; Iverson, 1992; Bonin et al. , 2006; Ernst found in domestic markets. However, et al. , 2006; Fritz and Havaš, 2007; van Dijk Pingleton (2009) noted that C. denticulata et al. , 2012), northern Argentina (Ernst et al. , was usually preferred as food over 2006; Fritz and Havaš, 2007; van Dijk et al. , C. carbonaria in areas where the two are 2012), Ecuador and Peru (King and Burke, sympatric, and Strong (2006) considered the 1989; Iverson, 1992; Ernst et al. , 2006; Fritz impacts of hunting overall to be and Havaš, 2007). Introduced populations insufficiently known. were reported to occur on several Caribbean islands (Bonin et al. , 2006; van Dijk et al. , C. carbonaria was also reported to be 2012). By using projected range maps, commonly captured and kept as a pet in Buhlmann (2009) estimated the total range many range countries (IUCN/SSC Tortoise 2 of the species to be 6 232 342 km . and Freshwater Turtle Specialist Group, 2012), and it was also considered popular in

the international pet trade (Senneke and transported to Suriname, where they were 8 Tabaka, 2003) due to its relatively small size, sold in the domestic market or exported. attractive coloration and hardiness Duplaix (2001) considered the smuggling of (Pingleton, 2009; Spiess, 1997). Spiess (1997) reptile species between the three countries reported that capture for export had a to be common. negative impact on populations, although not as significant as hunting for food. In the A positive opinion for specimens up to 7 cm 1990s, substantial increases in trade levels plastron length was formed at SRG16. were thought to potentially cause No information was identified on the captive population depletion (WCMC et al., 1993). production or ranching for the species in Adult individuals available for sale were Suriname. reported to be most commonly of wild- All reptiles in Suriname appear to be caught origin (Pingleton, 2009). Vinke and protected under the Game Law , apart from Vinke (2010) believed that wild-caught those designated as game species, ‘cage animals were also laundered amongst species’ (to be trapped alive) or harmful C. carbonaria exported as “farm-bred” and species, for which seasons and bag sizes are that exports of captive-produced tortoises of established (Suriname, 1954). C. carbonaria this species were subject to corruption and is classified as a ‘cage species’ and a bag limit lack of controls (Vinke and Vinke, 2008). In of two individuals and a seasonal hunting general, imported wild-caught tortoises were closure from August to December applies in considered susceptible to health problems, the northern region (Ministerie van RGB, whereas captive-bred and ranched 2013). No bag limits or seasonal hunting specimens were thought to generally be closures apply for the southern zone of the healthy (Pingleton, 2009). country (Ministerie van RGB, 2013).

Suriname Within Suriname, the species was reported to occur on the coastal areas as well as in the southern part of the country (Pingleton, 2009). The distribution maps of Walker (1989) and Iverson (1992) displayed several occurrence records on the northern half of the country, and one on the southern tip. C. carbonaria was reported to be found predominantly in the savannah areas of Suriname, with densities being much lower in forested areas (Pritchard, 1979).

No information was located on the species’ conservation status in Suriname.

The species’ population in Suriname was believed to have been subject to substantial declines due to the levels of international trade, which was highlighted to take place without assessment of the sustainability of trade and potential future effects (Vinke and Vinke, 2008). The IUCN/SSC Tortoise & Freshwater Turtle Specialist Group (2012) pointed out that individuals collected in Guyana and French Guyana were

References 9

Bonin, F., Devaux, B. and Dupré, A. (2006). Turtles of the world . London, UK: A&C Black. Buhlmann, K. A., Akre, T. S. B., Iverson, J. B., Karapatakis, D., Mittermeier, R. A., Georges, A., Rhodin, A. G. J., van Dijk, P. P. and Gibbons, J. W. (2009). A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conservation and Biology , 8 (2), p.116–149. Van Dijk, P. P., Iverson, J. B., Shaffer, H. B., Bour, R. and Rhodin, A. G. J. (2012). Turtles of the World , 2012 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. Rhodin, A. G. J., Pritchard, P. C. H., van Dijk, P. P., Saumure, R. A., Buhlmann, K. A., Iverson, J. B. and Mittermeier, R. A. (eds.). Chelonian Research Monographs , 5, Chelonian Research Foundation, p.243–328. Duplaix, N. (2001). Evaluation of the animal and plant trade in the Guianas: preliminary findings . (March). [Online]. Available at: http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Evaluation+of+the+ani mal+and+plant+trade+in+the+Guianas+-+preliminary+findings#0 [Accessed: 4 February 2013]. Ernst, C. H., Altenburg, R. G. M. and Barbour, R. W. (2006). Turtles of the World . p.-. [Online]. Available at: http://nlbif.eti.uva.nl/bis/turtles.php [Accessed: 1 May 2014]. Farias, I. P., Jerozolimski, A., Melo, A., das Neves Viana, M., Martins, M. and dos Santos Monjeló, L. A. (2007). Population genetics of the Amazonian tortoises, Chelonoidis denticulata and C. carbonaria , (Cryptodira: Testudinidae) in an area of sympatry. Amphibia-Reptilia , 28, p.357–365. Fritz, U. and Havaš, P. (2007). Checklist of chelonians of the world. Vertebrate Zoology , 57 (2), p.148–368. Garstecki, T. (2006). Evaluating imports of captive-bred or ranched wildlife specimens: guidelines for CITES Scientific Authorities of the EU Member States . Brussels, Belgium: TRAFFIC Europe. Hernández, O. (1997). Reproduccion y crecimiento del Morrocoy, Geochelone (Chelonoidis) carbonaria (Spix, 1824) (Reptilia, Testudinidae). Biollania , 13, p.165–183. Hernández, O. and Boede, E. O. (2008). Relación entre el tamaño de hembra y la producción de huevos en el Morrocoy sabanero Geochelone (Chelonoidis ) carbonaria (Spix, 1824) en un zoocriadero commercial de Venezuela. Interciencia , 33, 461-466. IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. (2012). Chelonoidis carbonaria. Draft species assessment . Iverson, J. B. (1992). A revised checklist with distribution maps of the turtles of the world . Richmond, USA: Earlham College. Kaur, K. (2011). Chelonoidis carbonaria Red-footed tortoise, in Animal Diversity Web . [Online]. Available at: http://animaldiversity.ummz.umich.edu/accounts/Chelonoidis_carbonaria/ [Accessed: 1 May 2014]. King, F. W. and Burke, R. L. (1989). Crocodilian, tuatara, and turtle species of the world: a taxonomic and geographic reference . Washington DC: Association of Systematics Collections, p.-216. Le, M., Raxworthy, C. J., McCord, W. P. and Mertz, L. (2006). A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution , 40 (2), p.517–531. Lowman, R. J. (1996). The captive mainenance and propagation of Redfooted and Yellowfooted Tortoises. Reptiles Magazine, 4(12), 48-63. Ministerie van RGB. (2013). Jachtkalender (Suriname). Ministerie van Ruimtelijke Ordening, Grond- en Bosbeheer . [Online]. Available at: http://www.gov.sr/sr/ministerie-van- rgb/documenten/jachtkalender.aspx [Accessed: 22 April 2014]. Ojasti, J. (1996). Wildlife utilization in Latin America: Current situation and prospects for sustainable management . Rome, Italy: Food and Agriculture Organisation of the United Nations.

Pingleton, M. (2009). The redfoot manual - a beginner’s guide to the redfoot tortoise . Champaign, 10 Illinois: Art Gecko Publishers. Pritchard, P. C. H. (1979). Encyclopedia of turtles . Neptune, USA: TFH Publishing Inc. Senneke, D. and Tabaka, C. (2003). Red-foot tortoises (Geochelone carbonaria) species care sheet . p.-. [Online]. Available at: http://www.chelonia.org/Articles/redfootcare.htm [Accessed: 1 May 2014]. Spiess, P. (1997). The Red-footed tortoise ( Geochelone carbonaria ), a South American treasure. Reptile and Amphibian Magazine , March/Apri, p.-. [Online]. Available at: http://www.kingsnake.com/rockymountain/RMHPages/RMHredfoot.htm [Accessed: 1 May 2014]. Strong, J. N. (2005). Seed dispersal and the ecological implications of hunting Geochelone carbonaria and G. denticulata in northwestern Brazil . Biotropica, 38(5), 683-686. Suriname. (1954). Jachtwet G.B. 1954 no. 25, including amendments G.B. 1954 no. 106, G.B. 1971 no. 61, S.B. 1980 no. 99, S.B. 1980 no. 116, S.B. 1982 no. 159 en S.B. 1994 no. 54, S.B. 1997 no. 33 . Vargas-Ramírez, M., Maran, J. and Fritz, U. (2010). Red- and yellow-footed tortoises, Chelonoidis carbonaria and C. denticulata (Reptilia: Testudines: Testudinidae), in South American savannahs and forests: do their phylogeographies reflect distinct habitats? Organisms Diversity & Evolution , 10, p.161–172. Vinke, T. and Vinke, S. (2008). Köhlerschildkröten – billige Massenware oder vom Aussterben bedroht? Schildkroeten im Fokus , 5 (3), p.28–31. Vinke, T. and Vinke, S. (2010). Do breeding facilities for chelonians threaten their stability in the wild. Schildkröten im Fokus , p.1–18. [Online]. Available at: http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Do+breeding+facilities +for+chelonians+threaten+their+stability+in+the+wild+?#0 [Accessed: 14 February 2013]. Walker, P. (1989). Geochelone carbonaria - Red-footed tortoise . Swingland, I. R. and Klemens, M. W. (eds.). Gland, Switzerland: IUCN/SSC Tortoise and Freshwater Turtle Specialist Group; The Durrell Institute of Conservation and Ecology, p.17–19. WCMC, IUCN/SSC and TRAFFIC. (1993). Significant trade in wildlife: a review of selected animal species in CITES Appendix II . Cambridge, UK: Draft report to the CITES Animals Committee.

Appendix 11 Table 1: Purpose of trade

Code Description

T Commercial

Z Zoo

G Botanical garden

Q Circus or travelling exhibition

S Scientific

H Hunting trophy

P Personal

M Medical (including biomedical research)

E Educational

N Reintroduction or introduction into the wild

B Breeding in captivity or artificial propagation

L Law enforcement / judicial / forensic

Table 2: Source of specimens

Code Description

W Specimens taken from the wild

R Ranched specimens: 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

D Appendix-I animals bred in captivity for commercial purposes in operations included in the Secretariat's Register, in accordance with Resolution Conf. 12.10 (Rev. CoP15), and Appendix-I plants artificially propagated for commercial purposes, as well as parts and derivatives thereof, exported under the provisions of Article VII, paragraph 4, of the Convention

A Plants that are artificially propagated in accordance with Resolution Conf. 11.11 (Rev. CoP15), as well as parts and derivatives thereof, exported under the provisions of Article VII, paragraph 5 (specimens of species included in Appendix I that have been propagated artificially for non-commercial purposes and specimens of species included in Appendices II and III)

C Animals bred in captivity in accordance with Resolution Conf. 10.16 (Rev.), as well as parts and derivatives thereof, exported under the provisions of Article VII, paragraph 5

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.), as well as parts and derivatives thereof

U Source unknown (must be justified)

I Confiscated or seized specimens (may be used with another code)

O Pre-Convention specimens