UNEP-WCMC technical report

Review of selected subject to long- standing import suspensions

Part III: , , and Central and South America and the Caribbean

(Version edited for public release)

Review of selected species subject to long-standing import suspensions. Part IIII: Europe, North America, and Central and South America and the Caribbean

Prepared for The European Commission, Directorate General Environment, Directorate E - Global & Regional Challenges, LIFE ENV.E.2. – Global Sustainability, Trade & Multilateral Agreements, Brussels,

Prepared May 2016

Copyright European Commission 2016

Citation UNEP-WCMC. 2016. Review of selected species subject to long-standing import suspensions. Part III: Europe, North America, and Central and South America and the Caribbean. UNEP-WCMC, Cambridge.

The UNEP World Conservation Monitoring Centre (UNEP-WCMC) is the specialist biodiversity assessment of the United Nations Environment Programme, the world’s foremost intergovernmental environmental organization. The Centre has been in operation for over 30 years, combining scientific research with policy advice and the development of decision tools.

We are able to provide objective, scientifically rigorous products and services to help decision-makers recognize the value of biodiversity and apply this knowledge to all that they do. To do this, we collate and verify data on biodiversity and ecosystem services that we analyze and interpret in comprehensive assessments, making the results available in appropriate forms for national and international level decision-makers and businesses. To ensure that our work is both sustainable and equitable we seek to build the capacity of partners where needed, so that they can provide the same services at national and regional scales.

The contents of this report do not necessarily reflect the views or policies of UNEP, contributory organisations or editors. The designations employed and the presentations do not imply the expressions of any opinion whatsoever on the part of UNEP, the European Commission or contributory organisations, editors or publishers concerning the legal status of any country, territory, city area or its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of a commercial entity or product in this publication does not imply endorsement by UNEP.

UNEP World Conservation Monitoring Centre (UNEP-WCMC) 219 Huntingdon Road, Cambridge CB3 0DL, UK UNEP promotes Tel: +44 1223 277314 environmentally sound www.unep-wcmc.org practices globally and in its own activities. Printing on paper from environmentally sustainable forests and recycled fibre is encouraged.

Contents

Introduction and summary…………………………………………………………………………………………………..………1 Ateles geoffroyi II/B ...... 3 Chiropotes chiropotes II/B ...... 15 Pithecia pithecia II/B ...... 18 Deroptyus accipitrinus II/B ...... 20 Paleosuchus trigonatus II/B ...... 24 Boa constrictor II/B ...... 28 Gopherus berlandieri II/B...... 33 nivalis II/B...... 38 Orchis mascula II/B ...... 42 mirabile II/B ...... 45 Cyclamen pseudibericum II/B ...... 47 Appendix ...... 49

Introduction

Introduction and summary

This document provides reviews of 21 species/country combinations of species from Europe, North America, and Central and South America and the Caribbean currently subject to long-standing Article 4.6(b) import suspensions. The document is provided to inform discussions by the Scientific Review Group as to whether these trade restrictions may still be warranted.

Trade data were downloaded on 10/03/20161 and the full dataset is available here: http://wcmc.io/SRG_76_direct_trade and http://wcmc.io/SRG_76_indirect_trade.

1 Data for the review of Deroptyus accipitrinus from Suriname was downloaded on the 31/03/2016. 1 Introduction

2 Ateles geoffroyi

PRIMATES: ATELIDAE Ateles geoffroyi II/B

COMMON NAMES: Geoffroy's Spider Monkey (EN), Atèle de Geoffroy (FR), Ateles de Geoffroy (ES)

RANGE STATES: Belize, Colombia (uncertain), Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, Panama

UNDER REVIEW: Belize, Colombia, Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Panama

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Belize, Colombia, Costa Rica, El Salvador, Guatemala, Honduras, Mexico and Panama first applied on 22/12/1997 and last confirmed on 28/05/2015.

Current no opinion i) for wild imports from Nicaragua applied 07/12/2012.

IUCN: Endangered

Taxonomic note The of Ateles geoffroyi has been subject to debate in the literature (Kellogg and Goldman, 1944; Rylands et al., 2006; Morales-Jimenez et al., 2015) and is considered to be in need of further taxonomic revision (Morales-Jimenez et al., 2015). The current CITES Standard Reference (Wilson and Reeder, 2005) recognises four subspecies (A. geoffroyi grisescens, A. g. ornatus, A. g. vellerosus, and A. g. yucatanensis), whereas other recent sources typically recognise seven subspecies (e.g. Rylands et al., 2006, Cuarón et al., 2008a, Mittermeier et al., 2013).

Although A. g. frontatus and A. g. panamensis are listed separately in CITES Appendix I, A. g. panamensis is generally considered a synonym of A. g. ornatus (Wilson and Reeder, 2005; Rylands et al., 2006, Morales-Jimenez et al., 2015). The adoption of Rylands et al., (2006) as the CITES Standard Reference for Ateles geoffroyi would result in the following taxonomic change: Ateles geoffroyi panamensis (Appendix I) will become A. g. ornatus. This review does not further refer to A. g. frontatus (Appendix I).

For the purposes of this review, the taxonomy accepted by the CITES Standard Reference is followed, but for clarification, the taxa used in the literature is given in square brackets. Trade patterns Ateles geoffroyi was listed in Appendix II on 04/02/1977 as part of the order level listing for Primates and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997, also as part of the order level listing for Primates. Subspecies A. g. frontatus and A. g. panamensis were listed in Appendix I on 01/07/1975 and in Annex A of the EU Wildlife Trade Regulations on 01/06/1997.

Belize: Belize has not published annual export quotas for A. geoffroyi for the period 2005-2016. Belize has submitted annual reports for all years 2005-2012 but has not yet submitted annual reports for 2013 or 2014.

3 Ateles geoffroyi

No direct exports of A. geoffroyi from Belize to the EU-28 were reported for the period 2005-2014. Direct trade in A. geoffroyi from Belize to countries other than the EU-28 2005-2014 comprised wild-sourced specimens for scientific purposes reported in 2009 (70) and in 2010 (350), by the exporter only.

No indirect trade in A. geoffroyi to the EU-28 originating in Belize was reported for the period 2005-2014. No direct or indirect exports of A. g. frontatus or A. g. panamensis from, or originating in Belize, to the EU-28 or the rest of the world was reported 2005-2014.

Colombia: Colombia has not published annual export quotas for A. geoffroyi for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

No direct or indirect trade in A. geoffroyi, A. g. frontatus or A. g. panamensis from, or originating in, Colombia to the EU-28 or the rest of the world was reported 2005-2014.

Costa Rica: Costa Rica has not published annual export quotas for A. geoffroyi for the period 2005-2016. Costa Rica has submitted annual reports for all years 2005-2014.

Direct exports of A. geoffroyi from Costa Rica to the EU-28 comprised 100 wild-sourced specimens for scientific purposes, reported by importers in 2014 (Table 1). Direct exports of A. geoffroyi from Costa Rica to countries other than the EU-28 comprised very low levels of wild-sourced derivatives and specimens traded for scientific purposes in 2005. No indirect trade of A. geoffroyi originating in Costa Rica to the EU-28 was reported for the period 2005-2014.

No direct or indirect trade to the EU-28 in A. g. frontatus or A. g. panamensis was reported 2005-2014. Direct exports of A. g. frontatus to countries other than the EU-28 from Costa Rica comprised low levels of trade of wild-sourced specimens for scientific purposes.

Table 1: Direct exports of Ateles geoffroyi from Costa Rica to the EU-28 (EU) and the rest of the world (RoW), 2005-2014. All trade was wild- sourced for scientific purposes.

Importer Term (unit) Reported by 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 EU specimens Importer 100 Exporter 200 RoW derivatives Importer Exporter 10 specimens (l) Importer 0.2 Exporter specimens Importer Exporter 20 11 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016 (and updated following receipt of Costa Rica’s 2014 annual report).

El Salvador: El Salvador has not published annual export quotas for A. geoffroyi for the period 2005- 2016. El Salvador has submitted annual reports for all years 2005-2014 with the exception of 2013 for which a report has not yet been received.

No direct trade in A. geoffroyi from El Salvador to the EU-28 was reported 2005-2014. Direct trade of A. geoffroyi from El Salvador to the rest of the world comprised 30 wild-sourced specimens for scientific purposes in 2007, reported by the exporter only. No indirect trade of A. geoffroyi originating in El Salvador to the EU-28 was reported for the period 2005-2014.

No direct or indirect exports of A. g. frontatus or A. g. panamensis from, or originating in, El Salvador to the EU-28 or the rest of the world was reported 2005-2014. 4 Ateles geoffroyi

Guatemala: Guatemala has not published annual export quotas for A. geoffroyi for the period 2005-2016 and has submitted annual reports for all years 2005-2013. Guatemala has not yet submitted an annual report for 2014.

Direct exports of A. geoffroyi from Guatemala comprised four live captive-bred (source C) individuals for circuses and travelling exhibitions in 2005 (Table 2). Direct exports of A. geoffroyi from Guatemala to countries other than the EU-28 comprised low levels of trade in live captive-bred individuals. Wild- sourced specimens for scientific purposes and very low levels of trade of bones of captive-bred animals for scientific purposes were also reported. No indirect trade of A. geoffroyi originating in Guatemala to the EU-28 was reported for the period 2005-2014.

No direct or indirect exports of A. g. frontatus or A. g. panamensis from, or originating in, Guatemala to the EU-28 or the rest of the world was reported 2005-2014.

Table 2: Direct exports of Ateles geoffroyi from Guatemala to the EU-28 (EU) and the rest of the world (RoW), 2005-2014. No trade was reported 2012-2014.

Importer Term (unit) Purpose Source Reported by 2005 2006 2007 2008 2009 2010 2011 EU live Q C Importer Exporter 4 RoW bones S C Importer Exporter 3 live Q C Importer Exporter 4 16 S C Importer Exporter 8 T C Importer 6 Exporter 6 Z C Importer 16 Exporter 6 specimens S W Importer Exporter 100 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016.

Honduras: Honduras has not published annual export quotas for A. geoffroyi for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

No direct or indirect trade in A. geoffroyi (including in Appendix-I listed A. g. frontatus or A. g. panamensis) from, or originating in, Honduras to the EU-28 or the rest of the world was reported 2005- 2014.

Mexico: Mexico has not published annual export quotas for A. geoffroyi for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

Direct exports from Mexico to the EU-28 consisted of 330 wild-sourced specimens for scientific purposes, reported in 2011 only by Mexico (Table 3). Direct exports from Mexico to the rest of the world comprised low levels of wild-sourced specimens for scientific purposes reported in 2009, 2013 and 2014. No indirect trade in A. geoffroyi to the EU-28 originating in Mexico was reported for the period 2005- 2014.

No direct or indirect exports of A. g. frontatus or A. g. panamensis from, or originating in, Mexico to the EU-28 or the rest of the world was reported 2005-2014.

5 Ateles geoffroyi

Table 3: Direct exports of Ateles geoffroyi from Mexico to the EU-28 (EU) and the rest of the world (RoW), 2009-2014. No trade was reported 2005- 2008.

Importer Term (unit) Purpose Source Reported by 2009 2010 2011 2012 2013 2014 EU specimens S W Importer Exporter 330 RoW specimens S W Importer 68 100 Exporter 68 100 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016.

Panama: Panama has not published annual export quotas for A. geoffroyi for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

No direct trade of A. geoffroyi from Panama to the EU-28 was reported 2005-2014. Direct exports of A. geoffroyi from Panama to the rest of the world 2005-2014 comprised 500 wild-sourced specimens for scientific purposes in 2010, reported by Panama only. No indirect trade in A. geoffroyi to the EU-28 originating in Panama was reported for the period 2005-2014.

No direct or indirect exports of A. g. frontatus or A. g. panamensis from, or originating in, Panama to the EU-28 or the rest of the world was reported 2005-2014. A. geoffroyi, was reported to occur in a range of forest habitats including primary and secondary lowland rainforests, evergreen, semi-deciduous and deciduous forest, cloud forests and mangrove swamps (Mittermeier et al., 2013). It occurs from southern and eastern regions of Mexico through the highlands of Guatemala into Belize, El Salvador and Honduras, to Nicaragua and Costa Rica, and to the forested regions of Panama and north western Colombia (Rylands et al., 2006; Cuarón et al., 2008a; Mittermeier et al., 2013).

A. g. grisescens was reported to occur in Rio Tuyra and through the Serranía del Sapo in south eastern Panama and the Cordillera de Baudó of north western Colombia (Kellogg and Goldman, 1944), although its occurrence in Colombia has later been questioned (Defler et al., 2003).

Kellogg and Goldman (1944) noted that A. g. ornatus [A. g. panamensis] occurred in Panama east of the Cordillera de San Blas, through Chiriquí and in western Costa Rica. Cuarón et al., (2008a) reported that A. g. ornatus [A. g. azuerensis] occurred on the western side of the forested mountains of the Azuero peninsula and [A. g. ornatus] in the forests of Panama, east of the Cordillera San Blas, west through Chiriquí to central western Costa Rica (Kellogg and Goldman, 1944; Cuarón et al., 2008a).

A. g. vellerosus was noted to occur in the Veracruz and eastern San Luis Potosí, Tabasco, Isthmus of Tehuantepec in eastern Oaxaca in Mexico and the highlands of Mexico and through El Salvador and Honduras (Kellogg and Goldman, 1944; Cuarón et al., 2008a; Mittermeier et al., 2013). A. g. yucatanensis was noted to occur in the Yucatán peninsula, north eastern Guatemala, Belize and in Campeche in southern Mexico (Rylands et al., 2006; Cuarón et al., 2008a).

Females reportedly reach sexual maturity at around four (Wainwright, 2007) to six and a half years old (Mittermeier et al., 2013) and breed every two to four years (Reid, 2009). The species was reported to have a low reproductive output, making replenishment of depleted populations difficult (Wainwright, 2007). It was considered probable that wild A. geoffroyi live “into their late 20s or early 30s” (Aureli and Schaffner, 2010).

6 Ateles geoffroyi

A. geoffroyi was reported to require sizeable tracts of undisturbed forests (Reid, 2009). Despite its reported occurrence in some large areas of suitable habitat, A. geoffroyi was classified by the IUCN as Endangered in 2008 due to severe habitat loss across its range, and the population was considered to be declining (Cuarón et al., 2008a). The species was estimated to have “declined by as much as 50% over the course of 45 years”, equivalent to three generations (Cuarón et al., 2008a). Previously, A. geoffroyi was classified as Vulnerable (1982-1994), Lower Risk/least concern (1996-2000) and as Least Concern (2003) (Cuarón et al., 2008a). The IUCN does not recognise A. g. panamensis as a subspecies, but considers it as a synonym of A. g. ornatus which was categorised as Endangered in 2008 due to past and future decline “expected to exceed 50 per cent in 45 years” (Cuarón et al., 2008c).

Although reported to be “relatively common in some protected areas across its range (Mittermeier et al., 2013), A. geoffroyi was described as “generally uncommon” (Reid, 2009) and it has been reported as locally extinct in some areas (Mittermeier et al., 2013). No estimates of global population size were found. The population of A. g. azuerensis was reported to number only 112-116 individuals (Mendez- Carvajal, Ruiz-Bernard, Franco and Silva, in prep. In: Cuarón et al., 2008a); estimates for other subspecies are available only for specific locations.

The main threat facing A. geoffroyi was reported to be habitat loss and fragmentation (Mittermeier et al., 2013; Cuarón et al., 2008a). The species was also reportedly affected by hunting for the pet trade and meat (Mittermeier et al., 2013), as well as medicinal use (Hines, 2005; Cuarón, 1991 & Silva-López, 1987 in Ceballos, 2014).

Given that Ateles geoffroyi sensu lato is in need of taxonomic revision, and that there may be little concordance between phylogenetically distinct units and the various described subspecies (which have been traditionally recognised by their country of origin and pelage colour and patterning) (Morales- Jimenez et al., 2015), there may be lookalike issues in determining subspecies in trade. For example, A. g. panamensis (Appendix I) occurs in Panama, as does A. g. grisescens (Appendix II).

Belize: Matmoros and Seal (2001) noted that A. g. yucatanensis was the only subspecies present in Belize and reported it to occurr in fragmented areas in the north as well as south of the Rio Bravo around the Bladen River, Chiquibul National Park, Lagoon Bank and in western Belize. The species was reported to be present within three protected areas: Upper Bladen [south central Belize] (Matamoros and Seal, 2001), Chiquibul Protected Area (comprised of the Chiquibul Forest Reserve and the Chiquibul National Park) (Hubrecht 1986; Waters and Ulloa, 2007) and Runaway Creek Nature Reserve, a protected area of 24.69 km2 (Hartwell et al., 2014). Hartwell et al. (2014) noted there were at least three groups of A. geoffroyi [A. g. yucatanensis] within Runaway Creek Nature Reserve, which were connected to a larger population to the east and south of the reserve. Rodríquez-Luna et al. (1996) noted that A. geoffroyi [A. g. vellerosus] was previously present in Colombia River Forest Reserve, but local people reported the species to have been extirpated from the area around 1980.

No estimates of the total population of Belize were found. A survey of the Runaway Creek Nature Reserve in 2007-2009, reported two groups of A. g. yucatanensis, consisting of 31 and 33 individuals (Notman and Pavelka, 2010). Hubrecht (1986) reported a population density of 19.6 [A. g. yucatanensis] individuals per km2 in Chiquibul Forest Reserve, which was considered to suggest that there was a “reasonable sized population of A. g. yucatanensis in the Bladen foothills” following a yellow fever epidemic in 1958 which was thought to have caused a population reduction.

In Belize, A. geoffroyi was reported to be threatened by forest clearance and capture of young individuals for trade (Wildtracks, 2013). The national Wildlife Protection Act (Chapter 20) prohibits hunting of A. geoffroyi (Law Revision Commissioner, 2000) and it is illegal to keep primates as pets in the country (Wildtracks, 2013). Furthermore, Matamoros and Seal (2001) reported A. geoffroyi [A. g. yucatanensis] to be in local trade, and that this trade contributed to a “perceived or inferred population decline”. 7 Ateles geoffroyi

Colombia: Only one subspecies, A. g. grisescens, has been reported to occur in Colombia (Kellogg and Goldman, 1944; Hernández-Camacho and Cooper, 1976 [A. paniscus grisescens]), although its current occurrence in the country is uncertain (Defler et al., 2003; Rylands et al., 2006).

Hernández-Camacho and Cooper (1976) noted that A. g. grisescens [A. paniscus grisescens] occurred only in the vicinity of Juradó very near the Panamanian border on the Pacific coast, restricted by the Baudó Mountains to a narrow coastal strip that may extend as far south as Cabo Corrientes. However, Defler et al. (2003) reported that there was no recent information regarding the presence of A. g. grisescens along the Panamanian border, noting that if the subspecies did occur in the region, the population would be small and endangered. Defler et al. (2003) reported that there were no specimens or observations to confirm the existence of A. g. grisescens in Colombia as suggested by Kellogg and Goldman (1944) and Hernández-Camacho and Cooper (1976).

In support of Defler et al.'s (2003) consideration that A. geoffroyi may no longer occur in Colombia, the IUCN Red List assessment for A. g. grisescens noted that Panama was the only range state for the subspecies (Cuarón et al., 2008d).

Costa Rica: Two or possibly three subspecies were reported to occur in Costa Rica. A. g. ornatus was reported to occur in central western Costa Rica (Rylands et al., 2006; Cuarón et al., 2008a), as was A. g. panamensis (see above proposed nomenclature changes) (Kellogg and Goldman, 1944). A. g. azuerensis was also found to occur near the Panama-Costa Rica border (Cuarón et al., 2008a; Mittermeier et al., 2013). A. g. ornatus [A. g. panamensis] has also been reported in central western Costa Rica (Kellogg and Goldman, 1944). A. geoffroyi [A. g. geoffroyi] was also reported to possibly extend into northern Costa Rica (Rylands et al., 2006; Cuarón et al., 2008a; Mittermeier et al., 2013).

The species has been reported to occur up to an altitude of 2800 m, mostly in large protected areas of primary forests (Wainwright, 2007). However, it was reportedly lost from many regions where it was once common, including protected areas such as Cabo Blanco Reserve, Finca La Pacifica and parts of Monteverde (Wainwright, 2007). Mittermeier et al. (2013) noted that A. g. ornatus occurred in 22 protected areas.

A. geoffroyi was reported to be “uncommon” in Costa Rica (Wainwright, 2007). Transect surveys (direct counts) of the 500 ha Punta Leona private wildlife refuge in 1996 reported a density of 0.036 individuals per ha (Timmock and Vaughan, 2002). Based on this population estimate, Timmock and Vaughan (2002) noted that there should be 11 individuals in the refuge, although as only four individuals had been directly observed, considered the estimates to be high. In the same area in 2006, Van Hulle and Vaughan (2009) observed 36 A. geoffroyi; they estimated the population size to be 15 individuals with a population density of 0.04 individuals per ha.

Weghorst (2007) reported high density estimates of A. geoffroyi at Sirena Biological Station, Corcovado National Park. The study involved walking twelve line transects (with a combined distance of 16.16 km) 35 times each and taking direct counts of A. geoffroyi (Weghorst, 2007). Estimates reported to vary from 51.53 – 142.87 individuals per km2 depending on whether effective, mean or maximum distances were used to estimate transect width (Weghorst, 2007).

Surveys were carried out in three forest fragments in 1999 at La Suerte biological field station, which was reported to be a government protected area (Pruetz and Leasor, 2002). No individuals of A. geoffroyi were observed during transects in the smallest forest of 15 ha, six individuals per km2 were observed in the second forest fragment (a logged area of 35 ha), and a minimum of eight to ten individuals were reported for the third area (pristine forest covering 100 ha) (Pruetz and Leasor, 2002).

Wainwright (2007) reported that, in some regions, A. geoffroyi used to be captured for the pet trade and that the species was heavily hunted in many regions. 8 Ateles geoffroyi

Costa Rican Law 9106 (2012) bans sport hunting of all wildlife, allowing only hunting for the purposes of population control and subsistence (Asamblea Legislativa de la República de Costa Rica, 2012). Law 9106 also prohibits the collection of wildlife (except for breeding in authorised centres) and the keeping of wildlife as pets (except when originating in legal breeding facilities) (Asamblea Legislativa de la República de Costa Rica, 2012).

El Salvador: A. g. vellerosus was noted to be the only subspecies present in El Salvador (Kellogg and Goldman, 1944; Cuarón et al., 2008a). In 1995, the species was reported to occur in “Nancuchiname, La Normandía and Cerro El Mono in the Department of Usulután [south eastern El Salvador], in Conchagua in the east of the Department of La Unión” [south eastern El Salvador] (López-Zepeda, 1995 in Morales-Hernández, 2002), and also in Montecristo National Park in the Department of Santa Ana [northern El Salvador] (J. Latin pers. comm. 2002 in Morales-Hernández, 2002). The density, habits and viability of the species in El Salvador were reported to be poorly known (Garber et al., 2006; Morales- Hernández, 2002). Garber et al. (2006) noted that populations existed in fragmented habitats.

Morales-Hernández (2003) undertook surveys of the species in the Chaguantique in the Munciplaity of Puerto El Triunfo and El Tercio in the Municiplaity of Jiquilisco in 2002. In the 350 km2 forest fragement of Chaguantique in which A. geoffroyi occurs, Morales-Hernández (2003) estimated the population to be 28 individuals with a density of 0.008 individuals per km2; in El Tercio (which has an area of 332.5 km2) 45 individuals were recorded at a density of 0.0135 per km2. However, in 2015, Giron, (2015) noted that the species was only present in one small and fragmented population in the Bahía de Jiquilisco Biosphere Reserve.

A. geoffroyi was categorised as Endangered in the 2009 list of threatened species of El Salvador (Ministerio de Medio Ambiente y Recursos Naturales, 2009),

The species forest habitats were reported to be threatened by deforestation (Estrada et al., 2006). It is prohibited to kill, destroy, damage or commercialise nationally Endangered species or to trade Endangered species without a permit (La Asamblea Legislativa de la Republica de El Salvador, 1994).

Guatemala: A. g. vellerosus [A. g. vellerosus and A. g. pan] and A. g. yucatanensis have been reported to occur in Guatemala (Kellogg and Goldman, 1944), with A. g. vellerosus reported from the highlands [southern Guatemala] (Kellogg and Goldman, 1944; Rylands et al., 2006; Mittermeier et al., 2013) and A. g. yucatanensis reported from north eastern Guatemala (Rylands et al., 2006; Cuarón et al., 2008a; Mittermeier et al., 2013).

The species was reported to occur at altitudes between 100 and 2000 m, but was considered most abundant between 100 and 300 m (Silva-López et al., 1998). In 1998, Silva- López et al. (1998) noted that the species occurred in six protected areas: Biotopo Cerro Cahuí, the archeological site of Ceibal, the Maya Biosphere Reserve, the National Park of Tikal, the Biotopo San Miguel la Palotada and the Sierra de la Minas Biosphere Reserve, across three regional Departments: Petén, Izabal and Zacaapa. In 1995 the species was reported to be found in Rio Dulce National Park (Silva-López et al. 1995 in Cuarón et al., 2008a) and in 1998, Silva-López et al. (1998) noted that the species might also occur in Cerro San Gil, a Watershed Protection Reserve [eastern Guatemala].

Silva-López et al. (1998) considered the species to be Vulnerable in Guatemala according to the IUCN criteria.

In a 5 km2 study area of undisturbed rain forest in Tikal National Park in northern Guatemala, Estrada et al. (2004) reported that the density of A. g. vellerosus was 56.4 individuals per km2, based on transect surveys carried out in 2002. Estrada et al. (2004) reported that 99 distinct subgroups were recorded within the study area.

9 Ateles geoffroyi

A. geoffroyi was reported to be threatened by hunting for meat and capture for pet markets (Silva-López et al., 1998). In 2009, The National Council of Protected Areas (CONAP, 2009) classed A. g. yucatanensis in Category 2: species in serious danger, which includes species that have been endangered by loss of habitat, trade, those with very small populations and endemic species with limited distributions. According to Article 24 of Decree 4-89, the species in Category 2 can only be used for scientific and research purposes and breeding for conservation purposes (CONAP, 2009; Congreso de la República de Guatemala, 1989). The harvest, capture, hunting, transport, exchange, trade and export of species included in the Endangered species list is prohibited by Articles 26 and 27 of Decree 4-89 although trade is permitted for second generation captive bred animals in cases where the facility and breeders are authorized (Congreso de la República de Guatemala, 1989).

Honduras: One subspecies A. g. vellerosuswas reported to occur in Honduras (Kellogg and Goldman, 1944; Cuarón et al., 2008a). Occurrence was reported on the north coast to the lowlands of the Mosquitia in the department of Gracias a Dios (Rylands et al., 2006) including Río Plátano Biosphere Reserve, as well as in Parque Nacional Pico Bonito in Atlántida Department (Hines, 2002 in Hines, 2005). Rylands et al. (2006) reported that the species of the Ateles had been very poorly documented in Honduras.

Hines (2005) carried out the first study of A. geoffroyi in Honduras, in Parque Nacional Pico Bonito, Atlántida, but reported that it was not possible to calculate population densities. A mean subgroup size of 6.93 individuals was found, which was reported to be larger than nearly all subgroup sizes reported elsewhere in Central and South America, with the exception of Panama (Hines, 2005).

Populations of Ateles spp. were reported to exist in fragmented habitats in Honduras (Garber et al., 2006), with habitat loss, fragmentation, and hunting for food, medicine and the pet trade cited as the largest threats for Ateles species in the country (Hines, 2005). Hines (2005) noted that hunting was prohibited in protected areas, although this was poorly enforced, and that the remoteness of core areas in large protected areas such as Parque Nacional Pico Bonito and Río Plátano Biosphere Reserve had helped to prevent overexploitation of the species.

Mexico: Two subspecies have been reported to occur in Mexico A. g. vellerosus was reported from coastal forests of south eastern Mexico (Ceballos, 2014), including southern Tamaulipas to Chiapas (Estrada and Coates-Estrada, 1984) in the region of La Huasteca, within San Luis Potosí and Veracruz (Estrada and Coates-Estrada, 1989 in Ceballos, 2014). A. g. yucatanensis was reported to be restricted to the forests of the Yucatán Peninsula (Kellogg and Goldman, 1944, Rylands et al., 2006; Mittermeier et al., 2013). During surveys of the Yucatán Peninsula in 1984, Watts et al., (1986) verified the presence of A. geoffroyi [A. g. yucatanensis] in Quintana Roo and Campeche, and noted that populations had also been reported in Yucatán. Garber et al. (2006) noted that populations of Ateles existed in fragmented habitats in the country.

The species was reported to occur from sea level to an altitude of 1500 m, although most locations were reported to be at an altitude of 700 m (Ceballos, 2014). Small numbers of individuals have also been reported in cacao, coffee and mixed plantations (Estrada and Coates-Estrada, 1996).

Estrada and Coates-Estrada (1996) estimated the population size of A. geoffroyi [A. g. yucatanensis] to be 400-600 individuals across 126 forest fragments and 44 agricultural sites at Los Tuxtlas, southern Veracruz. Estrada et al. (2004) carried out surveys of A. g. yucatanensis within a one km2 study area in a protected forest reserve at the Mayan site of Yaxchillán in the state of Chiapas identifying 17 individuals. A further survey within a 5 km2 site at the Mayan site of Calakmul found nine subgroups of the subspecies, with density of 17.2 individuals per km2 (Estrada et al., 2004).

10 Ateles geoffroyi

A. geoffroyi was classified as ‘in danger of extinction’ in Mexico (SEMARNAT, 2010; CONABIO, 2011). It was reported to be the primate species in Mexico “most rapidly affected by habitat loss and fragmentation” (Estrada and Coates-Estrada, 1996) due to the species’ requirement for large areas of habitat (Duarte-Quiroga and Estrada, 2003).

Several authors have reported a declining population trend for species of Ateles, predominately due to habitat destruction, including A. g. vellerosus (Estrada and Coates-Estrada, 1984) and A. g. yucatanensis (Watts et al., 1986). Estrada and Coastes-Estrada (1984) reported that “many populations of A. geoffroyi had been exterminated from areas where they were previously sympatric with Alouatta”.

In Mexico the species was reported to be threatened by poaching, the pet trade, and the use of its fat for traditional medicine (Cuarón, 1991 & Silva-López, 1987 in Ceballos, 2014). A. geoffroyi was reported to be the most common species of pet monkey identified as part of a survey in Mexico City (Duarte-Quiroga and Estrada, 2003). Since Mexican law reportedly forbids the commercialisation of wild primates, and no breeding centres exist in Mexico, it was considered that all pets of the species in the country were obtained illegally (Duarte-Quiroga and Estrada, 2003). The species was reported to occur in several large protected areas that support viable populations, including Sian Kaan in Quintana Roo, Calakmul in Campeche, and Montes Azules in Chiapas (Ceballos, 2014).

Panama: Two subspecies of A. geoffroyi were reported to occur in Panama. A. g. ornatus [A. g. azuerensis] was reported to occur in the forested mountains on the western side of the Azuero peninsula in south western Panama (Rylands et al., 2006; Mittermeier et al., 2013; Méndez-Carvajal, 2013) as well as the forested regions east of the Cordillera San Blas and west though Chiriquí (Cuarón et al., 2008a; Mittermeier et al., 2013). A. g. grisescens was reported to occur in the lower basin of the Río Tuira in Panama (Matamoros and Seal, 2001; Rylands et al., 2006; Mittermeier et al., 2013), and probably through the Serranía del Sapo of extreme southeast Panama (Rylands et al., 2006; Cuarón et al., 2008a; Mittermeier et al., 2013). Cuarón et al. (2008a) reported that A. geoffroyi [all subspecies] occurred in over 23 protected areas in Panama.

A. geoffroyi was assessed as Endangered in Panama (República de Panamá, 2008). A total of 124 individuals of A. g. ornatus [A. g. azuerensis] were detected on the Azuero Peninsula based on direct and indirect counts, from which 145 individuals were estimated to remain in the wild in 13 localities in the Azuero Peninsula (Méndez-Carvajal, 2013). This included 74 individuals [A. g. azuerensis] in the southern and eastern regions of the Azuero peninsula within gallery and secondary woodland (occurrence was confirmed in Venao, La Zahina, Cañas, Flores de Tonosi, Pedasi district, La Miel, Las Tablas and the Tonosi Valley) (Méndez-Carvajal, 2013). A conservative estimate of a further 50 individuals within isolated areas in western region of the peninsula, in gallery forest was made (Méndez-Carvajal, 2013). The peninsula was reported to be severely deforested and populations were described as “remnant and diminished” in Veraguas and Los Santos provinces and extinct in the Herrera province Méndez-Carvajal (2013).

A small reintroduced population of 28 individuals of A. geoffroyi was reported to be present on Barro Colorado Island, with a density of 0.17 individuals per ha (Milton and Hopkins, 2006). This reintroduction reportedly occurred in the early 1960’s after the species was hunted to extinction on the island (Mittermeier and Fleagle, 1976). It was reported that only five of the original eighteen individuals released survived beyond the mid-1960s (Milton and Hopkins, 2006).

There was reported to be a long history of collection of Ateles spp. from several regions in Panama since the early 20th century (Hines, 2005). Méndez-Carvajal, (2013) considered that that A. g. ornatus [A. g. azuerensis] was threatened by deforestation, poaching and illegal trade in Panama. No information on the management of the species in Panama was found. References

11 Ateles geoffroyi

Asamblea Legislativa de la República de Costa Rica 2012. Reformes y adiciones a la ley de conservación de vida silvestre, ley No 7317, de 30 de Octubre de 1992. Available at: http://faolex.fao.org/docs/pdf/cos122976.pdf. [Accessed 07/03/2016] La Asamblea Legislativa de la Republica de El Salvador 1994. Ley de conservación de vida silvestre. Decreto No. 844. Aureli, F. and Schaffner, C.M. 2010. Spider monkeys. Current Biology, 20(15): R624–R626. Cant, J.G.H. 1978. Population survey of the spider monkey Ateles geoffroyi at Tikal, Guatemala. Primates, 19: 525–535. Ceballos, G. 2014. Mammals of Mexico. John Hopkins University Press, Baltimore, . Coehlo, A.M.J., Coehlo, L., Bramblett, C., Bramblett, S. and Quick, L.B. 1976. Ecology, population characteristics, and sympatric associations in primates: a sociobioenergetic analysis of howler and spider monkeys in Tikal, Guatemala. Yearbook of Physical Anthropology, 20: 96–135. CONABIO 2011. Fichas de especies prioritarias. Mono Araña (Ateles geoffroyi). 1-5 pp. Available at: http://www.biodiversidad.gob.mx/especies/especies_priori/fichas/pdf/monoArana.pdf. [Accessed 07/03/2016] CONAP 2009. Lista de Especies Amenazadas de Guatemala -LEA. Documento técnico 67 (02-2009). Congreso de la República de Guatemala 1989. Ley de Áreas protegidas, Decreto No. 4-89. 24 pp. Available at: http://mcd.gob.gt/wp-content/uploads/2013/07/GUA-Decreto-4-89-Ley-Areas-Protegidas1.pdf. [Accessed 07/03/2016] Cuarón, A.D. 1991. Conservación de los primates y sus hábitats en el sur de México. Universidad Nacional, San José, Costa Rica. Cuarón, A.D., Morales, A., Shedden, A., Rodriguez-Luna, E., de Grammont, P.C. and Cortés-Ortiz, L. 2008a. Ateles geoffroyi. The IUCN Red List of Threatened Species 2008. Available at: http://www.iucnredlist.org/details/2279/0. [Accessed: 27/10/2015]. Cuarón, A.D., Morales, A., Shedden, A., Rodríguez-Luna, E. and de Grammont, P.. 2008b. Ateles geoffroyi ssp. frontatus. Available at: http://www.iucnredlist.org/details/2280/0. [Accessed: 7/03/2016]. Cuarón, A.D., Morales, A., Shedden, A., Rodríguez-Luna, E. and de Grammont, P.C. 2008c. Ateles geoffroyi ssp. ornatus. Available at: http://www.iucnredlist.org/details/summary/2289/0. [Accessed: 7/03/2016]. Cuarón, A.D., Morales, A., Shedden, A., Rodríguez-Luna, E. and de Grammont, P.. 2008d. Ateles geoffroyi ssp. grisescens In: IUCN 2008. IUCN Red List of Threatened species. Available at: http://www.iucnredlist.org/details/2287/0. [Accessed: 22/01/2016]. Defler, T.R., Rodríguez-M, J. V. and Hernández-Camacho, I.J. 2003. Conservation priorities for Colombian primates. Primate Conservation, 19: 10–18. Duarte-Quiroga, A. and Estrada, A. 2003. Primates as pets in Mexico City: an assessment of the species involved, source of origin, and general aspects of treatment. American Journal of Primatology, 61(2): 53–60. Estrada, A. and Coastes-Estrada, R. 1984. Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico. American Journal of Primatology, 7: 133– 137. Estrada, A. and Coates-Estrada, R. 1989. La destrucción de la selva y la conservacion de los primatres silvestres de mexico (Alouatta y Ateles). In: Estrada, A., López-Wilchis, R. and Coates-Estrada, R. (Eds.). Prrimatología en México: Comportamiento, Ecología, Apprvechamiento y Conservación de Primates. Universidad Autónoma, Metropolitana, México. 211–233. Estrada, A. and Coates-Estrada, R. 1984. Some observations of the present distribution and conseravtion of Alouatta and Ateles in southern Mexico. American Journal of Primatology, 7: 133–137. Estrada, A. and Coates-Estrada, R. 1996. Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. International Journal of Primatology, 17(5): 759–783. Estrada, A., Garber, P.A., Pavelka, M.S. and Luecke, L. 2006. Overview of the Mesoamerican primate fauna, primate studies, and conservation concerns. In: New Perspectives in the Study of Mesoamerican Primates. Springer, US. Estrada, A., Luecke, L., Van Belle, S., Barrueta, E. and Meda, M.R. 2004. Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys in the Mayan sites of Calakmul and Yaxchilán, Mexico and Tikal, Guatemala. Primates; Journal of Primatology, 45(1): 33–9. Garber, P.A., Estrada, A. and Pavelka, M.S.M. 2006. New perspectives in the study of Mesoamerican 12 Ateles geoffroyi

primates: concluding comments and conservation priorities. In: New perspectives in the study of Mesoamerican primates. Springer, US. 563–584. Giron, L. 2015. Geoffroy’s Spider Monkey (Ateles geoffroyi). Available at: http://www.speciesconservation.org/case-studies-projects/geoffroys-spider-monkey/4533. [Accessed: 29/10/2015]. Grimm, U. 2016. Ute Grimm ( CITES Scientific Authority) pers. comm to UNEP-WCMC, 13/03/2016. Hartwell, K.S., Notman, H., Boenfant, C. and Pavelka, M.S.M. 2014. Assessing the occurrence of sexual segregation in Spider Monkeys (Ateles geoffroyi yucatanensis), its mechanisms and function. International Journal of Primatology, 35: 425–444. Hernández-Camacho, J. and Cooper, R.W. 1976. The nonhuman primates of Colombia. In: R. W. Thorington, J. and Heltne, P.G. (Eds.). Neotropical Primates: Field Studies and Conservation. National Academy of Sciences, , DC. 35–69. Hines, J.J.H. 2002. Ateles geoffroyi in Northern Honduras: Feasibility Survey. Unpublished Masters Thesis. University of Toronto, Toronto. Hines, J.J.H. 2005. Ecology and taxonomy of Ateles geoffroyi in Parque Nacional Pico Bonito, Atlántida, Honduras. Australian National University. Hubrecht, R.C. 1986. Operation Raleigh primate census in the Maya Mountains, Belize. Primate Conservation, 7: 15–17. Van Hulle, M. and Vaughan, C. 2009. The effect of human development on mammal populations of the Punta Leona Private Wildlife Refuge, Costa Rica. Revista de biología tropical, 57(1-2): 441–9. J. Latin 2002. Wildlife Biologist, Director of Montecristo National Park, Santa Ana, El Salvador pers. comm. to in Morales-Hernández, 2002 Kellogg, R. and Goldman, E.A. 1944. Review of the spider monkeys. Proceedings of the United States National Museum, 96: 1–45. Law Revision Commissioner 2000. Belize Wildlife Protection Act Chapter 20. López-Zepeda, E. 1995. Plan de Manejo de la Reserva Natural Estricta de Conchagua. Ministerio de Obras Públicas, Dirección General de Caminos. San Salvador, El Salvador. Matamoros, Y. and Seal, U.S. 2001. Informe Final. Taller para la Conservación Asesoramiento y Manejo Planificado para los Primates Mesoamericanos, Parque Zoológico Simón Bolívar, San José, Costa Rica, 23-25 Junio 1997. IUCN/SSCConservation Breeding Specialist Group (CBSG. Apple Valley, Minnesota, USA. Méndez-Carvajal, P.G. 2013. Population size, distribution and conservation status of howler monkeys (Alouatta coibensis trabeata) and spider monkeys (Ateles geoffroyi azuerensis) on the Azuero Peninsula, Panama. Primate Conservation, 26(1): 3–15. Milton, K. and Hopkins, M.E. 2006. Growth of a reintroduced spider monkey (Ateles geoffroyi) population on Barro Colorado Island, Panama. In: New Perspectives in the Study of Mesoamerican Primates. Springer, US. 417–435. Ministerio de Medio Ambiente y Recursos Naturales 2009. Diario oficial – San Salvador, 5 de Junio 2009, tomo No. 383. Mittermeier, R.A. and Fleagle, J.G. 1976. The locomotor and postural repertoires of Ateles geoffroyi and Colobus guereza, and a reevaluation of the locomotor category semibrachiation. American Journal of Physical Anthropology, 45(2): 235–253. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. 2013. Handbook of the mammals of the world. Vol. 3 Primates. Lynx Edicions, Barcelona, . Morales-Hernández, K. 2002. Wild populations of spider monkeys (Ateles geoffroyi) in El Salvador, Central America. Neotropical Primates, 10: 153–154. Morales-Hernández, V.K. 2003. Estudio Preliminar de la Poblacion de Ateles geoffroyi ‘Mono Araña’ en Chaguantique y El Tercio. Universidad de El Salvador, San Salvador, El Salvador. Morales-Jimenez, A.L., L., C.-O. and A., D.F. 2015. Phylogenetic relationships of Mesoamerican spider monkeys (Ateles geoffroyi): Molecular evidence suggests the need for a revised taxonomy. Molecular Phylogenetics and Evolution, 82: 484–494. Naturales, M. de M.A. y R. 2009. Acuerdo No 36 - listado oficial de especies de vida silvestre amenazadas o en peligro de extinción. Notman, H. and Pavelka, M.S.M. 2010. Demography, diet and range size in a population of Black-handed Spider Monkey’s. In: The International Primatological Society (IPS) congress. Available at: 13 Ateles geoffroyi

http://primate-society.com/ips/public/ips_program/IPS10-663.pdf. Pruetz, J.D. and Leasor, H.C. 2002. Survey of three primate species in forest fragments at La Suerte biological field station, Costa Rica. Neotropical Primates, 10(1): 4–9. Reid, F. 2009. A field guide to the mammals of Central America and Southeast Mexico. Second. Oxford University Press, USA, , NY. 384 pp. República de Panamá 2008. Autoridad Nacional del ambiente (ANAM) Resolución No. AG - 0051-2008. Annex 1. Rodríquez-Luna, E., Cortés-Ortiz, L., Mittermeier, R., Rylands, A., Wong-Reyes, G., Carrillo, E., Matamoros, Y., Nuñez, F. and Motta-Gill, J. 1996. Hacía un plan de acción para los primates mesoamericanos. Neotropical Primates, 4: 119–133. Rylands, A.B., Groves, C.P. and Mittermeier, R.A. 2006. Taxonomy and Distributions of Mesoamerican Primates. 29–79. SEMARNAT 2010. NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, protección ambiental - especies nativas de México de flora y fauna silvestres - categorías de riesgo y especificaciones para su inclusión, exclusión o cambio - lista de especies en riesgo. DIARIO OFICIAL, 1: 1–78. Silva-López, G. 1987. La situación actual de los monos araña (Atles geoffroyi) y alludar (Alouatta palliata) en la Sierra de Santa Marta (Vera Cruz, México. Universidad Veracruzana, Xalapa, Veracruz. Silva-López, G., Motta-gill, J. and Sánchez-Hernández, A.I. 1998. Distribution and status of the primates of Guatemala. Primate Conservation, 18: 30–41. Timmock, J. and Vaughan, C. 2002. A census of mammal populations in Punta Leona Private Wildlife Refuge, Costa Rica. Revista de Biología Tropical, 50: 1169–1180. Wainwright, M. 2007. The mammals of Costa Rica. A natural history and field guide. Comstock Publishing Associates. Waters, S.S. and Ulloa, O. 2007. Preliminary survey of the current distribtuion of primates in Belize. Neotropical Primates, 14(2): 80–82. Watts, E.S., Ric-Gray, V. and Chan, C. 1986. Monkeys of the Yucatan Peninsula, Mexico: preliminary survey of their distribution and status. Primate Conservation, 7: 17–22. Weghorst, J.A. 2007. High population density of black-handed spider monkeys (Ateles geoffroyi) in Costa Rican lowland wet forest. Primates, 48: 108–116. Wildtracks 2013. Primate Rehabilitation Centre. Information Pack. Available at: http://www.wildtracksbelize.org/resources/primate_rehab_info_pack_20130709.pdf. [Accessed 07/03/2016] Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed. The John Hopkins University Press, Baltimore, USA. 2142 pp.

14 Chiropotes chiropotes

PRIMATES: PITHECIIDAE Chiropotes chiropotes II/B

COMMON NAMES: Tawny-olive bearded Saki (EN), Saki barbudo de dorso rojo (ES), Saki du Rio Negro (FR)

RANGE STATES: Brazil, Guyana, French Guiana [FR], Suriname, Venezuela (Bolivarian Republic of)

UNDER REVIEW: Guyana

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Guyana first applied on 30/04/2004 and last confirmed on 28/05/2015, replacing a Negative opinion applied 04/02/2002.

Current No opinion i) for wild imports from Brazil first applied 16/02/2010, replacing previous Article 4.6(b) suspension for Brazil applied 22/12/1997.

IUCN: Least Concern

Taxonomic note Chiropotes chiropotes was elevated from the subspecies C. satanas chiropotes in 2003 based on karyotypic and molecular evidence (Bonvicino et al., 2003); C. chiropotes was further split into C. chiropotes and C. israelita. The CITES Standard Reference for mammals considers C. chiropotes, C. israelita and C. santanas to be distinct species (Wilson and Reeder, 2005). Trade patterns Chiropotes chiropotes was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the order listing for Primates.

Guyana have submitted annual reports for all years 2005-2014. Guyana has not published annual export quotas for C. chiropotes for the period 2005-2014.

Direct exports of C. chiropotes from Guyana to the EU-28 2005-2014 comprised 12 live, wild-sourced individuals for commercial purposes (reported by Guyana) and six live individuals for zoos (reported by the importer), all of which were wild-sourced and reported in 2010 (Table 1). Direct trade in C. chiropotes from Guyana to countries other than the EU-28 2005-2014 also primarily comprised low levels of live, wild-sourced individuals for the purpose of commercial trade in the period 2008-2011. In addition, low levels of trade in specimens for commercial and scientific purposes to countries other than the EU was reported in 2010.

There was no indirect trade in C. chiropotes from Guyana to the EU-28 reported over the period 2005- 2014.

15 Chiropotes chiropotes

Table 1: Direct exports of Chiropotes chiropotes from Guyana to the EU-28 (EU) and the rest of the world (RoW), 2005-2014. All trade was in wild individuals. No trade was reported 2005-2007 or 2012-2014. Quantities have been rounded to two decimal places, where appropriate.

Importer Term Unit Purpose Reported by 2008 2009 2010 2011 EU live - T Importer Exporter 12 Z Importer 6 Exporter RoW live - T Importer 13 12 Exporter 50 3 58 12 Z Importer 29 Exporter specimens l T Importer Exporter 0.01 - S Importer 25 Exporter T Importer 25 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016. Conservation status Chiropotes chiropotes has been reported in Brazil (states of Amazonas and Roraima in the north) and in the Bolivarian Republic of Venezuela, in the Bolívar state in the south, with a distribution bounded by the rivers Orinoco, Branco and Negro (Mittermeier et al., 2013). It has also been recorded as occurring in Suriname, French Guiana and the south of Guyana (Hollowell and Reynolds, 2005; Petter and Desbordes, 2013).

C. chiropotes has been recorded in transitional semi-deciduous tropical moist forest (Mittermeier et al., 2013). Home ranges have been recorded as 1.22 km²on forested islands (Mittermeier et al., 2013), and up to 5.59 km2 in continuous forest (Boyle et al., 2009), with group sizes of up to 35 individuals recorded (Boyle and Smith, 2010). Chiropotes species have been reported to have a five month gestation period, producing one infant (Petter and Desbordes, 2013). C. chiropotes [C. s. chiropotes] has been estimated to have birth intervals of at least 24 months (Peetz, 2001 in Mittermeier et al., 2013). Individuals reach sexual maturity at approximately 3 years (Mittermeier et al., 2013).

The species was categorised as Least Concern by the IUCN as it had a wide range in a relatively undisturbed area (Veiga et al., 2008).

Veiga et al. (2008) reported that there were no major threats to the species, although some subsistence level hunting occurred. Habitat fragmentation has been noted as a potential threat to the species due to its large home range size (Boyle and Smith, 2010).

Guyana: No information on the specific distribution of C. chiropotes (as the subspecies C. s. chiropotes) in Guyana was found. A 1995 survey recorded Chiropotes satanas [prior to the elevation of C. satanas chiropotes to species level] in the southern and eastern part of the country, east of the Essequibo River and south-east of the Rupununi River (Sussman and Phillips-Conroy, 1995); a later survey recorded that the extent of the species’ northerly range had diminished, and that it no longer extended north as far as the coast (Lehman et al., 2006). A survey of 16 sites in Guyana during 1994-1997 observed C. satanas [which may have included C. chiropotes] in seven forest habitats, including rainforest, southern forest and mora forest (Lehman, 2004). They were found to have small geographic ranges and be habitat specialists in Guyana (Lehman, 2004). 16 Chiropotes chiropotes

C. chiropotes is not listed as a protected species under the Environmental Protection (Wildlife Management and Conservation) Regulations 2009, which covers the protection of wild and animals in Guyana.

No further information on the status, population size or management of the species in Guyana could be identified.

References Bonvicino, C.R., Boubli, J.P., Otazú, I.B., Almeida, F.C., Nascimento, F.F., Coura, J.R. and Seuánez, H.N. 2003. Morphologic, Karyotypic, and Molecular Evidence of a New Form of Chiropotes (Primates, Pitheciinae). American Journal of Primatology, 61(January): 123–133. Boyle, S.A., Lourenço, W.C., da Silva, L.R. and Smith, A.T. 2009. Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. International Journal of Primatology, 30(4): 515–531. Boyle, S.A. and Smith, A.T. 2010. Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia. Primates, 51(1): 43–51. Hollowell, T. and Reynolds, R.P. 2005. Checklist of the terrestrial vertebrates of the Guiana Shield. Bulletin of the Biological Society of Washington, 13: 1–106. Lehman, S.M. 2004. Biogeography of the primates of Guyana: Effects of habitat use and diet on geographic distribution. International Journal of Primatology, 25(6): 1225–1242. Lehman, S.M., Sussman, R.W., Phillips-Conroy, J. and Prince, W. 2006. Ecological Biogeography of Primates in Guyana. In: Lehman, S.M. and Fleagle, J.G. (Eds.). Primate Biogeography: Progress and Prospects. Springer US, New York. 105–130. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. 2013. Handbook of the mammals of the world. Vol. 3 Primates. Lynx Edicions, Barcelona, Spain. Peetz, A. 2001. Ecology and social organization of the bearded saki Chiropotes satanas chiropotes (Primates: Pitheciinae) in Venezuela. Ecotropical Monographs, 1: 1–170. Petter, J.J. and Desbordes, F. 2013. Primates of the world. Martin, R. (Ed.). Princeton University Press, Princeton and Oxford. 186 pp. Sussman, R.W. and Phillips-Conroy, J.E. 1995. A survey of the distribution and density of the primates of Guyana. International Journal of Primatology, 16(5): 761–791. Veiga, L.M., Silva Jr., J.S., Mittermeier, R.A.& and Boubli, J.P. 2008. Chiropotes chiropotes. The IUCN Red List of Threatened Species 2015. Available at: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T43891A10829879.en. [Accessed: 13/11/2015]. Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed. The John Hopkins University Press, Baltimore, USA. 2142 pp.

17 Pithecia pithecia

PRIMATES: PITHECIIDAE Pithecia pithecia II/B

COMMON NAMES: Pale-headed Saki (EN), Saki à tête pâle (FR), Saki de cara blanca (ES)

RANGE STATES: Brazil, French Guiana [FR], Guyana, Suriname, Venezuela (Bolivarian Republic of) UNDER REVIEW: Guyana

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Guyana first applied on 30/04/2004 and last confirmed on 28/05/2015, replacing the previous negative opinion formed on 04/02/2002.

Current no opinion for wild imports from Brazil formed on 27/01/1999.

IUCN: Least Concern

Taxonomic note Pithecia pithecia has been considered to be composed of two subspecies (P. pithecia pithecia and P. pithecia chrysocephala), however in a recent re-examination of the genus, P. chrysocephala was proposed as a distinct species, occurring only in Brazil (Marsh, 2014). The CITES Standard Reference recognises P. pithecia chrysocephala as a subspecies of P. pithecia (Wilson and Reeder, 2005). Trade patterns Pithecia pithecia was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the order listing for Primates. Guyana has submitted annual reports for all years 2005-2014 and has not published annual export quotas for P. pithecia for the period 2005- 2014.

No direct or indirect trade in P. pithecia originating in Guyana to the EU-28 or the rest of the world was reported over the period 2005-2014. Conservation status Pithecia pithecia has been reported as endemic to the Guiana Shield forests (Hollowell and Reynolds, 205) in eastern Venezuela, throughout Guyana, Suriname and French Guiana and in the north of Brazil, north of the Rio Amazonas (Eisenberg and Redford, 2000; Urbani, 2006; Mittermeier et al., 2013; Marsh, 2014).

P. pithecia is a Neotropical primate recorded as confined to multi-layered tropical evergreen forests (Eisenberg and Redford, 2000; Mittermeier et al., 2013). The species has been reported in disturbed habitat and forest fragments, and at higher densities in mature forest (Mittermeier et al., 2013). Home ranges have been estimated as 0.04-0.1 km² (Eisenberg and Redford, 2000; Mittermeier et al., 2013).

P. pithecia have been recorded to have an approximately 6-month gestation period, producing one infant (Eisenberg and Redford, 2000; Mittermeier et al., 2013).

The species was categorised as Least Concern by the IUCN as it had a wide range, was found in a number of protected areas, and did not appear to have any major threats (Marsh et al., 2015).

18 Pithecia pithecia

Pithecia spp. were reported to be threatened by habitat disturbance/fragmentation and hunting throughout their range for pets, subsistence food and trophies (Marsh, 2014).

Guyana: Pithecia pithecia has been reported throughout Guyana (Mittermeier and van Roosmalen, 1981; Sussman and Phillips-Conroy, 1995; Lehman et al., 2001; Lehman, 2004), mostly along tributary rivers in northern Guyana that descend to the coast, but also further inland such as the Rupununi River (Marsh, 2014). P. pithecia was reported to occur within the Iwokrama Reserve, central Guyana (Iwokrama International Centre for Rain Forest Conservation and Development, 1999).

The species is not listed as a protected species under the 2009 Environmental Protection (Wildlife Management and Conservation) Regulation, which covers the protection of wild plants and animals.

Surveys conducted 1994-1997 at 18 sites in Guyana recorded P. pithecia at 10 of the sites, with a total sighting rate of 2.05 groups/100 km (n = 24; Lehman et al., 2006).

No further information on the status, population size or management of the species in Guyana could be identified. References Eisenberg, J.F. and Redford, K.H. 2000. Mammals of the Neotropics. Volume 3: The central Neotropics - Ecuador, Peru, Bolivia, Brazil. University of Chicago Press. 609 pp. Hollowell, T. and Reynolds, R.P. 2005. Checklist of the terrestrial vertebrates of the Guiana Shield. Bulletin of the Biological Society of Washington, 13: 1–106. Iwokrama International Centre for Rain Forest Conservation and Development 1999. Mammals of Iwokrama. Available at: http://www.iwokrama.org/mammals/guides/prim1.html#pipi. [Accessed: 17/11/2015]. Lehman, S., Prince, W. and Mayor, M. 2001. Variations in group size in white-faced sakis (Pithecia pithecia): evidence for monogamy or seasonal congregations. Neotropical primates, 9(3): 96–101. Lehman, S.M. 2004. Biogeography of the primates of Guyana: Effects of habitat use and diet on geographic distribution. International Journal of Primatology, 25(6): 1225–1242. Lehman, S.M., Sussman, R.W., Phillips-Conroy, J. and Prince, W. 2006. Ecological Biogeography of Primates in Guyana. In: Lehman, S.M. and Fleagle, J.G. (Eds.). Primate Biogeography: Progress and Prospects. Springer US, New York. 105–130. Marsh, L.K. 2014. A taxonomic revision of the saki monkeys, Pithecia Desmarest, 1804. Neotropical Primates, 21(July): 1–163. Marsh, L.K., Mittermeier, R.A. and Veiga, L.. 2015. Pithecia pithecia. The IUCN Red List of Threatened Species 2015. Available at: http://dx.doi.org/10.2305/IUCN.UK.2015-1.RLTS.T43942A70609046.en. [Accessed: 16/11/2015]. Mittermeier, R.A. and van Roosmalen, M.G.M. 1981. Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatologica, 36(1-2): 1–39. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. 2013. Handbook of the mammals of the world. Vol. 3 Primates. Lynx Edicions, Barcelona, Spain. Sussman, R.W. and Phillips-Conroy, J.E. 1995. A survey of the distribution and density of the primates of Guyana. International Journal of Primatology, 16(5): 761–791. Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed. The John Hopkins University Press, Baltimore, USA. 2142 pp. Urbani, B. 2006. A survey of primate populations in northeastern Venezuelan Guayana. Primate Conservation, 20(20): 47–52.

19 Deroptyus accipitrinus

PSITTACIFORMES: PSITTACIDAE Deroptyus accipitrinus II/B

SYNONYMS Psittacus accipitrinus

COMMON NAMES: Hawk-headed Parrot (EN), Papegeai maillé (FR), Loro cacique (ES)

RANGE STATES: Brazil, Colombia, Ecuador, French Guiana (FR), Guyana, Peru, Suriname, Venezuela (Bolivarian Republic of). UNDER REVIEW: Suriname

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Suriname first applied on 30/04/2004 and last confirmed on 28/05/2015. Previous negative opinion formed on 05/09/2002.

Current no opinion for wild imports from Brazil formed on 16/11/1999.

Current no opinion i) for wild imports from Peru applied on 20/06/2011

IUCN: Least Concern

Trade patterns Suriname published annual export quotas for live Deroptyus accipitrinus every year 2005-2014. Trade appears to have been within quota in all years (Table 1).

Direct exports of D. accipitrinus from Suriname to the EU-28 2005-2014 comprised five live, wild- sourced individuals for commercial purposes (reported by Suriname), which were traded in 2010 (Table 2). Direct exports to countries other than the EU-28 comprised primarily of live, wild-sourced individuals for both commercial and breeding purposes. In addition, low levels of trade in live individuals for personal, scientific and zoological purposes, specimens for scientific and [erroneously] for breeding purposes, and feathers for scientific purposes were reported in 2005-2014 to countries other than the EU.

Indirect trade in D. accipitrinus originating in Suriname to the EU-28 2005-2014 consisted of one live, wild-sourced individual re-exported via in 2011 for zoos, reported by the exporter only. Table 1: CITES export quotas for wild-sourced Deroptyus accipitrinus from Suriname 2005-2014 and global direct exports, as reported by the countries of import and Suriname 2005-2014.

Years 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 Quota (wild-taken) 300 300 300 300 300 300 300 300 300 300 Reported by Importers 96 69 27 14 36 28 184 34 46 41 Reported by Exporter 57 100 65 76 55 38 127 132 294 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 31/03/2016.

20 Deroptyus accipitrinus

Table 2: Direct exports of wild-sourced Deroptyus accipitrinus from Suriname to the EU-28 and the rest of the world (RoW) 2005-2014.

Importer Term Unit Purpose Reported by 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 EU live - T Importer Exporter 5 RoW feathers - S Importer 40 Exporter 40 150 live - B Importer 20 14 74 24 Exporter 16 23 20 16 54 47 50 P Importer 6 Exporter S Importer Exporter 1 T Importer 56 46 27 14 36 14 104 10 46 41 Exporter 17 45 20 52 10 14 84 62 Z Importer Exporter 12 specimens - B Importer Exporter 3 - S Importer 3 Exporter 39 22 24 25 14 59 20 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 31/03/2016. Conservation status Deroptyus accipitrinus is a distinctive parrot generally found in pairs or small groups of 3-7 individuals, perched on exposed dead tree-tops (Juniper and Parr, 1998). D. accipitrinus has been mainly recorded within undisturbed ‘terra firme’ (subtropical/tropical moist lowland) forest, with occasional use of coastal sand-ridge and savanna forests (Collar and Boesman, 2016). It is found all year round across its range (Collar and Boesman, 2016).

There are two subspecies currently recognised. D. a. accipitrinus (Linneaus, 1758) is commonly known as the Northern Red-fan Parrot and ranges across south east Columbia to north east Peru, the Guianas and northern Brazil (Dickinson, 2003). D. a. fuscifrons (Hellmayr, 1905) is known as the Southern Red-fan Parrot and is found in central Brazil (south of the Amazon; Dickinson, 2003). D. a. fuscifrons can be distinguished morphologically from D. a. accipitrinus by the lack of a white patch on its brown forehead and crown (Juniper and Parr, 1998).

This taxon has been assessed by the IUCN as ‘Least Concern’ on account of its extremely large range of 4 240 000 km2(BirdLife International, 2012). The species population trend was reported to be decreasing (BirdLife International, 2012). It was reported that this species was likely to lose 24-31.3 per cent of suitable habitat within its distribution over three generations (23 years) based on a model of Amazonian deforestation (Soares-Filho et al., 2006; Bird et al., 2011). Given the species’ “tolerance of fragmentation/degradation/edge-effects and/or the extent of overall losses”, it was predicted to decline by less than 25 per cent over three generations (BirdLife International, 2012). The total population size has not been quantified (BirdLife International, 2012). Although Stotz et al. (1996) previously described this species as “fairly common”, De Oliveira Lunardi et al. (2003; cited in UNEP-WCMC, 2011) reported more recently that the population density was low, and that the species was “considered to be naturally rare in the wild”.

BirdLife International (2012) did not report any substantial threats to the species; however, habitat loss and harvesting have been found to impact this species. Specifically, it has been recorded that habitat loss is most severe through the east of the species’ range (south of the Amazon, in Pará and Maranhão), 21 Deroptyus accipitrinus

while in the west the species has been “overtrapped locally” for the pet trade (Collar and Boesman, 2016; Juniper and Parr, 1998). Ridgely (1981; cited in UNEP-WCMC, 2011) noted that although this species is in great demand for the pet trade, it has always been rare in captivity.

Suriname: Haverschmidt (1968) documented Deroptyus accipitrinus to be commonly found in the forests of sand ridges, in savannah forests, and in the interior of Suriname (cited in WCMC, IUCN/SSC Trade Specialist Group and TRAFFIC International, 1993). Donahue and Pierson (1982; cited in WCMC, IUCN/SSC Trade Specialist Group and TRAFFIC International, 1993) confirmed its common status. The species was still documented as common in 2007, with “more than 20 individuals encountered daily in prime habitat and season” (Braun et al., 2007). In 2011, a rapid biological assessment of the Kwamalasamutu region (southwestern Suriname) recorded the species in all three of its survey sites (Conservation International, 2011).

Fuller et al. (1987) reported that hunting and trade of native birds and mammals was prohibited in Suriname since 1970, with the exception of listed game or domestic species (cited in WCMC and IUCN/SSC Trade Specialist Group and TRAFFIC International, 1993).

The species was included within Phase II of the CITES Review of Significant Trade (RST) process at the 9th meeting of the Animals Committee (1993). A report produced as part of that process documented that there was “no clear biological justification” for the species’ annual export quotas, which ranged from 150 to 176 individuals between the years 1987 and 1992 (Thomsen, 1988; cited in WCMC, IUCN/SSC Trade Specialist Group and TRAFFIC International, 1993). The species was categorized as of “possible concern,” for Suriname, but no recommendations were formulated by the Animals Committee. No current information on the management of the species within Suriname was located.

References Bird, J.P., Buchanan, G.M., Lees, A.C., Clay, R.P., Develey, P.F., Yépez, I. and Butchart, S.H.M. 2012. Integrating spatially explicit habitat projections into extinction risk assessments: A reassessment of Amazonian avifauna incorporating projected deforestation. Diversity and Distributions, 18(3): 273– 281. BirdLife International 2012. Deroptyus accipitrinus. Available at: http://dx.doi.org/10.2305/IUCN.UK.2012-1.RLTS.T22686416A39056595.en. [Accessed: 18/01/2016]. Braun, M.J., Finch, D.W., Robbins, M.B. and Schmidt, B.K. 2007. A field checklist of the birds of Guyana. Washington D. C. Collar, N. and Boesman, P. 2016. Red-fan Parrot (Deroptyus accipitrinus). Available at: http://www.hbw.com/node/54760. [Accessed: 18/01/2016]. Conservation International 2011. A rapid biological assessment of the Kwamalasamutu Region, Suriname, August-September 2010. Preliminary Report. Conservation International. Dickinson, E.C. 2003. The Howard and Moore complete checklist of the birds of the world. 3rd Ed. Christopher Helm Publishers Ltd., London, UK. Donahue, P.K. and Pierson, J.E. 1982. Birds of Suriname, an annotated checklist. J. E. Pierson. Fuller, K.S., Swift, B., Jorgensen, A. and Brautigam, A. 1987. Latin American Wildlife Trade Laws. 2nd revis. World Wildlife Fund-US. 418 pp. Haverschmidt, F. 1968. Birds of Surinam. Oliver and Boyd, Edinburgh, London. Juniper, T. and Parr, M. 1998. Parrots: a guide to the parrots of the world. Pica Press, Robertsbridge, UK. de Oliveira Lunardi, V., Francisco, M.R., Rocha, G.T., Goldschmidt, B. and Galetti Junior, P.M. 2003. Karyotype description of two Neotropical Psittacidae species: the endangered Hyacinth Macaw, Anodorhynchus hyacinthinus, and the Hawk-headed Parrot, Deroptyus accipitrinus (Psittaciformes: Aves), and its significance for conservation plans. 283–287 pp. Ridgely, R.S. 1981. The current distribution and status of mainland and neotropical parrots. Parquier, R.F. (Ed.). ICBP Technical Publication No.1. Smithsonian Press. 233–384 pp. Soares-Filho, B.S., Nepstad, D.C., Curran, L.M., Cerqueira, G.C., Garcia, R.A., Ramos, C.A., Voll, E., McDonald, A., Lefebvre, P. and Schlesinger, P. 2006. Modelling conservation in the Amazon basin. Nature, 440(7083): 520–523. 22 Deroptyus accipitrinus

Stotz, D.F., Fitzpatrick, J.W., Parker, T.A. and Moskovits, D.K. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. Thomsen, J.B. 1988. Guyana and Suriname establish quotas on parrot exports. Parrotletter, 1(1): 11–12. UNEP-WCMC 2011. Review of American species/country combinations subject to long-standing import suspensions. Cambridge (UK). WCMC and IUCN/SSC Trade Specialist Group and TRAFFIC International 1993. Significant Trade in Wildlife: a Review of Select Animal Species in CITES Apppendix II. Draft report to the CITES Animals Committee, June 1993.

23 Paleosuchus trigonatus

CROCODYLIA: ALLIGATORIDAE Paleosuchus trigonatus II/B

SYNONYMS: Caiman trigonatus, Crocodilus trigonatus, Paleosuchus niloticus, Paleosuchus trigomatus

COMMON NAMES: Schneider's Smooth-fronted Caiman (EN), Caïman hérissé (FR), Caimán frentiplano (ES)

RANGE STATES: Bolivia (Plurinational State of), Brazil, Colombia, Ecuador, French Guiana [FR] Guyana, Peru, Suriname, Venezuela (Bolivarian Republic of)

UNDER REVIEW: Guyana

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Guyana first applied on 30/04/2004 and last confirmed on 28/05/2015. Previous negative opinion formed on 22/05/2003, previous positive opinion formed on 22/02/2000 and Article 4.6(b) import suspension formed 22/12/1997.

IUCN: Lower Risk/least concern (needs updating)

Trade patterns Paleosuchus trigonatus was listed in Appendix II on 01/07/1975 and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the order listing for Crocodylia.

Guyana has published annual export quotas of 1000 live wild-sourced P. trigonatus every year in the period 2005-2015, with the exception for 2014 when a quota was published for 1648 live individuals (Table 1). Trade appears to have been within quota every year according to both Guyana and importers (Table 1); Guyana has submitted annual reports for all years 2005-2014. Table 1: CITES export quotas for live, wild-sourced Paleosuchus trigonatus from Guyana 2005-2016, and global exports as reported by the countries of import and Guyana 2005-2014. Trade data for 2015-2016 are not yet available

2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 Quota 1000 1000 1000 1000 1000 1000 1000 1000 1000 1648 1000 1000 Importer 246 397 471 386 371 466 272 235 504 465 Exporter 293 428 575 745 369 450 344 463 219 469

Direct exports of P. trigonatus from Guyana to the EU-28 2005-2014 comprised low levels of live, wild- sourced individuals traded for commercial purposes; four live wild-sourced individuals were reported imported for commercial purposes (Table 2). No direct trade to the EU-28 has been reported since 2010. Direct trade in P. trigonatus from Guyana to countries other than the EU-28 comprised primarily of moderate levels of live wild-sourced individuals for commercial trade. In addition, 10 live source ‘I’ individuals were traded for commercial purposes in 2010, reported by the importer only.

24 Paleosuchus trigonatus

Indirect trade in P. trigonatus to the EU-28 originating in Guyana 2005-2014 consisted of two wild- sourced live individuals for circuses and travelling exhibitions, re-exported via in 2010. Table 2: Direct exports of Paleosuchus trigonatus from Guyana to the EU- 28 (EU) and the rest of the world (RoW), 2005-2014. Quantities have been rounded to two decimal places, where appropriate.

Importer Term (unit) Purpose Source Reported by 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 EU live T W Importer 4 Exporter 18 2 4 6 37 RoW bodies S W Importer 1 Exporter 1 live B W Importer Exporter 5 T I Importer 10 Exporter W Importer 246 397 471 382 371 466 272 229 504 465 Exporter 275 426 575 741 363 413 339 463 219 469 Z W Importer 6 Exporter specimens (l) S W Importer Exporter 0.01 specimens S W Importer 4 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016. Conservation status P. trigonatus is a small caiman with a reported average adult size of 100-130 cm (Brazaitis, 2001 in Trutnau and Sommerlad, 2006). The species was reported to occur in south eastern Colombia, eastern Ecuador, eastern Bolivia, eastern Venezuela, north eastern Peru, across Guyana, Suriname and French Guiana and in large parts of northern and central Brazil (Trutnau and Sommerlad, 2006). The species reportedly occurs in rainforests (Magnusson and Lima, 1991), close to waterfalls and rapids (Magnusson, 1992),

Magnusson and Lima (1991) estimated that females reach sexual maturity at 11 years old and males at 20 years old. Females were reported to incubate eggs for over 100 days (Magnusson et al., 1985), with an average clutch size of 17 (Groombridge, 1987).

P. trigonatus was assessed as Lower Risk/least concern by the IUCN, although it was noted in the assessment that it needed updating (Crocodile Specialist Group, 1996). Dieter (2000) reported that P. trigonatus had a low risk of extinction as a result of a wide range and local abundance. Magnusson and Campos (2010) reported there was poor availability of survey data for the species, but noted that populations of P. trigonatus appeared to be “healthy” throughout its range.

The main threats to P. trigonatus were reported to be destruction of habitat and subsistence hunting (Magnusson and Campos, 2010; Trutnau and Sommerlad, 2006). Unlike other species of crocodilians, the skins of P. trigonatus were reported to have low commercial value due to the small body size and highly armoured skin (Groombridge, 1987; Magnusson and Campos, 2010). Magnusson and Campos (2010) reported that due to the low commercial value, hunting of the species has predominately been on a subsistence basis and considered that the species had a low potential for sustainable management. The species was also reported to be traded for the pet trade, reaching prices of between US $150 and $300 per individual (Dieter, 2000). Magnusson, (pers. comm. to UNEP-WCMC, 2015) noted that “there is no reason to suspect that the species might be overexploited”. In addition, P. trigonatus was reported to be 25 Paleosuchus trigonatus

one of only two crocodilian species that was not under a conservation programme in any South American countries (Velasco, 2008).

Guyana: P. trigonatus has been recorded in Kabocalli, in the Iwokrama Forest (Bicknell et al., 2013) and in the Sipu-Acarai mountains, Kamoa River, Essequibo River and Sipu River (Señaris et al., 2007).

P. trigonatus was not listed as a protected species in the Wildlife Management and Conservation Regulations of 2013 under the Environmental Protection Act (Government of Guyana, 2013). The CITES Management Authority of Guyana was contacted for further information on the management and status of P. trigonatus in the country, but a response has not yet been received.

No estimates of population size in Guyana were found. One farm carrying out captive breeding and collection of hatchlings of P. trigonatus was reported to be present in Guyana in 1992 (Luxmoore, 1992).

Magnusson and Campos (2010) reported that only limited extraction of the species from the wild was permitted in Guyana, and that this was predominately for the pet trade, subject to a CITES quota. Klemm and Navid (1989) reported that licences could be obtained to take the species from the wild. Campos (pers. comm. to UNEP-WCMC, 2015) noted hunting pressure for crocodiles and deforestation of riparian forests on the Border of Brazil and Guyana in 2015. References Bicknell, J., Snyder, A., Lim, B., Horsley, T., Bryce, C. and Worthington, R. 2013. Monitoring biodiversity by Operation Wallacea in the Iwokrama and Surama Forests, Guyana. Operation Wallacea research report 2011-2013. 40 pp. Brazaitis, P. 2001. A guide to the identification of the living Species of Crocodilians. - Science Resource Center. The Wildlife Conservation Society. Originally prepared for the inaugural class of the AZA. Crocodile Management School. St Augustines Alligator farm, St August. Campos, Z.M.S. 2015. Zilca Maria Da Silva Campos, Researcher for Empresa Brasileira de Pesquisa Agropecuária (Brazilian Agricultural Research Corporation) pers. comm. to UNEP-WCMC 17th December 2015. Crocodile Specialist Group 1996. Paleosuchus trigonatus. Available at: http://www.iucnredlist.org/details/46588/0. [Accessed: 16/11/2015]. Dieter, C.T. 2000. The Ultimate Guide to Crocodilians in Captivity. 3rd Edition. Crocodile Encounter Publishing. Government of Guyana 2013. Environmental Protection (Wildlife Management and Conservation) Regulations, 2009. The Official Gazette of Guyana (legal supplement) B 16th November 2013. 177/2013. Government of Guyana National Printers Ltd, Georgetown. 137–183 pp. Groombridge, B. 1987. The distribution and status of world crocodilians. In: Webb, G.J.W., Manolis, S.C. and Whitehead, P.J. (Eds.). Wildlife Management: Crocodiles and Alligators. Surrey Beatty & Sons Pty Ltd, Chipping Norton, Australia. 9–22. de Klemm, C. and Navid, D. 1989. Crocodilians and the law. In: Crocodiles, their ecology management and conservation. A special publication of the IUCN/SSC Crocodile Specialist Group. IUCN, Gland, Switzerland. 80–100. Luxmoore, R.A. 1992. Directory of crocodilian farming operations. IUCN, Gland, Switzerland and Cambridge, UK. Magnusson, W. 2015. Bill Magnusson of Instituto Nacional de Pesquisas da Amazônia pers. comm to UNEP-WCMC 10th December 2015. Magnusson, W.E. 1992. Paleosuchus trigonatus. Catalogue of American Amphibians and Reptiles, 555: 1–3. Magnusson, W.E. and Campos, Z. 2010. Schneider’s Smooth-fronted Caiman Paleosuchus trigonatus. In: Manolis, S.C. and Stevenson, C. (Eds.). Crocodiles. Status Survey and Conservation Action Plan. Crocodile Specialist Group, Darwin. 43–45. Magnusson, W.E. and Lima, A.P. 1991. The Ecology of a Cryptic Predator, Paleosuchus trigonatus, in a Tropical Rainforest. Journal of Herpetology, 25(1): 41–48. Magnusson, W.E., Lima, A.P. and Sampaio, R.M. 1985. Sources of heat for nests of Paleosuchus

26 Paleosuchus trigonatus

trigonatus and a review of crocodilian nest temperatures. Journal of Herpetology, 19(2): 199–207. Señaris, J.C., Lasso, C.A., Rivas, G., Kalamandeen, M. and Marawaranu, E. 2007. Amphibians and Reptiles of the Acarai Mountains, and Sipu, Kamoa and Essequibo Rivers in the Konashen COCA, Southern Guyana. In: Alonso, L.E., McCullough, J., Naskrecki, P., Alexander, E. and Wright, H.E. (Eds.). A rapid biological assessment of the Konashen Community Owned Conservation Area, Southern Guyana. RAP Bulletin of Biological Assessment 51. Conservation International, Arlington, VA, USA. 55–62. Trutnau, L. and Sommerlad, R. 2006. Crocodilians. Their natural history and captive husbandry. Edition Chimaira, Frankfurt am Main, Germany. 646 pp. Velasco, A.B. 2008. Crocodile management, conservation and sustainable use in Latin America. IUCN. 72- 88 pp.

27 Boa constrictor

SQUAMATA: BOIDAE Boa constrictor II/B

SYNONYMS: Boa constrictor isthmica, Boa constrictor longicauda, Boa constrictor melanogaster, Boa constrictor nebulosa, Boa diviniloqua, Boa diviniloqua mexicana, Boa eques, Boa imperator, Boa mexicana, Boa orophias, Boa ortonii, Constrictor auspex, Constrictor constrictor, Constrictor diviniloquus, Constrictor formosissimus, Constrictor orophias, Constrictor rexserpentum, Epicrates sabogae

COMMON NAMES: Boa Constrictor (EN, FR, ES)

RANGE STATES: Argentina, Aruba, Belize, Bolivia (Plurinational State of), Brazil, Colombia, Costa Rica, Dominica, Ecuador, El Salvador, French Guiana [FR], Guatemala, Guyana, Honduras, Mexico, Nicaragua, Panama, Paraguay, Peru, Saint Lucia, Suriname, Trinidad and Tobago, Uruguay, Venezuela (Bolivarian Republic of) UNDER REVIEW: Honduras

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Honduras first applied on 22/12/1997 and last confirmed on 28/05/2015.

Current no opinion i) for wild imports from El Salvador applied on 20/06/2011.

Current no opinion i) for wild imports from Peru applied on 02/12/2011.

Current no opinion ii) for wild imports from Suriname applied on 28/05/2013.

Current no opinion for wild imports from Costa Rica applied on 22/02/2000.

IUCN: Not assessed

Taxonomic note McDiarmid et al. (1999) recognise 10 subspecies of Boa constrictor, of which three have been classified as island endemics, and a further two as regionally isolated (O’Shea, 2011). The number of B. constrictor subspecies, however, is highly disputed due to its high morphological and ecological variability (Henderson et al., 1995). The number of reported subspecies has ranged from eight to eleven (Peters and Orejas-Miranda, 1986; Henderson et al., 1995; O’Shea, 2011), with other studies arguing for the elevation of some subspecies to species level (Price and Russo, 1991). Rather than classifying by subspecies, Savage (2002) proposed classifying B. constrictor into four geographic variants or “races”. Trade patterns B. constrictor was listed in Appendix II on 01/07/1975 and in Appendix II on 04/02/1977 as part of the family listing for Boidae (with the exception of B. c. occidentalis which was listed in Appendix I on 22/10/1987). It was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997, also as part of a family listing.

Honduras has not published annual export quotas for B. constrictor for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

28 Boa constrictor

Direct exports of B. constrictor from Honduras to the EU-28 2005-2014 consisted primarily of moderate levels of live ranched individuals for commercial purposes, and wild specimens for scientific purposes during 2005-2007 (Table 1). Direct trade in B. constrictor from Honduras to countries other than the EU- 28 consisted primarily of moderate levels of live ranched or wild individuals for the purpose for commercial purposes during 2006-2006 (Table 1).

No indirect trade in B. constrictor from Honduras to the EU-28 was reported 2005-2014. Table 1: Direct exports of Boa constrictor from Honduras to the EU-28 and the rest of the world (RoW) 2005-2014. Importer Term Purpose Source Reported by 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 EU28 live T F Importer 1 Exporter R Importer 230 Exporter 660 specimens S W Importer 300 450 Exporter 300 RoW bodies - W Importer Exporter 4 live T R Importer 1200 Exporter 2080 W Importer 500 Exporter 3660 specimens - W Importer Exporter 2000 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016. Conservation status B. constrictor is a widespread species (Wilson and McCranie, 2004a) with a range across South and Central America, and into northern Mexico (McDiarmid et al., 1999). It is also reported to have established colonies in the United States of America (Snow et al., 2007) and to have colonised over 40 South and Central American islands, where it has often been classified as a pest species (Henderson et al., 1995; Porras, 1999; Boback, 2005; Quick et al., 2005), for example Cozumel Island, Mexico (Vázquez- Domínguez and Suárez-Atilano, 2012).

This species has been described as a habitat and dietary generalist (Henderson et al., 1995). It has been reported to be terrestrial, arboreal, and aquatic (Wilson and Townsend, 2006), and has been found in habitats ranging from humid to sub-humid forests, and from grasslands to deserts (Henderson et al., 1995). The species is reported as highly diverse morphologically (Henderson et al., 1995). Most adults range between 2-3 m in length (Savage, 2002), but maximum lengths of 4.5 m have been recorded (Savage, 2002), and many island population individuals are reportedly smaller than those on the neighbouring mainland (Boback, 2006). As with most Boidae species, B. constrictor shows female-biased sexual dimorphism (Price and Russo, 1991; Bertona and Chiaraviglio, 2003; Leenders and Watkins- Colwell, 2004), with adult females up to 14 per cent longer than males (Bertona and Chiaraviglio, 2003). Females are oviparous, and can lay 14-60 eggs in a clutch (Bertona and Chiaraviglio, 2003; Reed, 2005). When they hatch, neonates measure 0.3-0.5 m long (Quick et al., 2005; Pizzatto and Marques, 2007).

B. constrictor has not yet been assessed by the IUCN (IUCN, 2015) but it is reportedly common across much of its range (Wilson and Townsend, 2006; O’Shea, 2011). The species has been reported to be highly traded for the pet market (Green, 2011). Some subspecies, particularly island endemics, have been considered especially vulnerable to direct killing, as well as capture for trade due to their limited range sizes (Daltry, 2009; Green, 2011).

Honduras: B. constrictor is considered widespread across Honduras (Wilson and McCranie, 2004a), specifically the subspecies B. c. imperator, which has the broadest Central American range (O’Shea, 2011). It has been reported in a range of different habitat types at elevations up to 1370 m (Wilson and 29 Boa constrictor

McCranie, 2004b; Wilson and Townsend, 2006, 2007). In Honduran cloud forests, B. constrictor was reported as infrequent, but stable in lower montane wet forests (Wilson and McCranie, 2004b). It was reported as common and stable in lowland moist and premontane wet forests where it was found in 77 per cent (10/13) of localities surveyed (Wilson and Townsend, 2006), and common and widespread in upland pine-oak forests (Wilson and Townsend, 2007).

In northern Honduras, the species was reportedly rare but stable in the premontane wet forests of the Parque Nacional Pico Bonito McCranie and Castañeda, 2005) and it was confirmed as present across all five major islands in the Islas de la Bahia (the “Bay Islands”) (McCranie et al., 2005; Green, 2011). In western Honduras, the species was recorded as present in pine forest at elevation ~760 m around the Yellow River in Copan, (but not recorded in surveyed areas of cloud forest, coffee plantation, or pasture land in the area) (Castañeda and Marineros, 2013). B. constrictor was also recorded as present in Cerro Guanacaure and Cordillera de la Botija, both in southern Honduras (Green, 2011).

There is a specific morph of B. c. imperator, which is endemic to the Cayos Cochinos (Hog Islands) off the Caribbean coast of Honduras (Montgomery et al., 2015). Historically, this island morph has been highly threatened by poaching for the pet trade due to its distinct pink colouration and small body size (Reed et al., 2007). Thousands of individuals of this specific morph were reportedly removed from the islands in the 1970s-1980s (Porras, 1999; Reed et al., 2007), with very few mature individuals recorded by the late 1980s (Wilson and Cruz Diaz, 1993). Poaching has reportedly decreased substantially since the designation of the Cayos Cochinos Archipelago as a Natural Marine Monument in 2003 and the captive breeding of this morph in Europe and the United States of America, leading to increasing population sizes in recent years (Green, 2011; Montgomery et al., 2015). However, despite a low market price and the prohibition of exports from the island, it was reported that harvesting of wild populations continues at an unknown rate (Reed et al., 2007; Montgomery et al., 2015), and individuals are illegally traded (Green, 2011). In 2015, an “Assessment of the Impact of the Pet Trade” noted that a better understanding of the Cayos Cochinos morph, including its basic biology and the level and impact of current poaching, was required before sustainable management could be achieved (Montgomery et al., 2015). No non- detriment finding for exports of the Cayos Cochinos morph currently exists, therefore an export ban has been maintained (Montgomery et al., 2015).

B. constrictor is not subject to any quotas in Honduras and there is no information on management of the species was found. This species is found in several protected areas: the Pico Bonito National Park (McCranie and Castañeda, 2005), the National Marine Park of the Bay Islands (McCranie et al., 2005), and the Cayos Cochinos Archipelago National Marine Monument (Montgomery et al., 2015) where it is listed as a “conservation target” (HCRF/USAID, 2014). B. constrictor was included in Phase II of the CITES Review of Significant Trade (RST) process in 1993 (AC9), and the species was categorised as of “possible concern” for Honduras. A report produced as part of the RST concluded that there was “no indication that the recent level of trade in live animals and skins is a significant threat to the species as a whole”, however “local populations might be affected” (WCMC et al., 1993). No recommendations for Honduras were formulated by the Animals Committee. References Bertona, M. and Chiaraviglio, M. 2003. Reproductive biology, mating aggregations, and sexual dimorphism of the Argentine Boa Constrictor (Boa constrictor occidentalis). Journal of Herpetology, 37(3): 510–516. Boback, S.. 2006. A morphometric comparison of island and mainland boas (Boa constrictor) in Belize. Copeia, 2: 261–267. Boback, S.M. 2005. Natural history and conservation of island Boas (Boa Constrictor) in Belize. Copeia, 2005(4): 879–884. Castañeda, F. and Marineros, L. 2013. La Herpetofauna de la Zona de Río Amarillo, Copán, Honduras. Available at: http://190.11.224.74:8080/jspui/handle/123456789/1902. [Accessed: 13/11/2015]. 30 Boa constrictor

Daltry, J. 2009. The status and management of Saint Lucia’s forest reptiles and amphibians. Technical Report No. 2 to the National Forest Demarcation and Bio-Physical Resource Inventory Project, FCG International Ltd, Helsinki, Finland. Green, S.E.. 2011. Evolutionary biology and conservation of the Hog Island Boa Constrictor. PhD Thesis. University of Kent, Canterbury, UK. HCRF/USAID 2014. Plan de Manejo en el Monumento Natural Marino Archipiélago Cayos Cochinos, Honduras 2014-2025. Henderson, R.., Waller, T., Micucci, P., Puorto, G. and Bourgeois, R. 1995. Ecological correlates and patterns in the distribution of Neotropical boines (Serpentes: Boidae): a preliminary assessment. Herpetological Natural History, 3(1): 15–27. IUCN 2015. The IUCN Red List of Threatened Species. Version 2015.3. Available at: http://www.iucnredlist.org/. [Accessed: 3/12/2015]. Leenders, T. and Watkins-Colwell, G.J. 2004. Notes on a collection of amphibians and reptiles from El Salvador. Postilla, 231(231). McCranie, J.R. and Castañeda, F.E. 2005. The herpetofauna of Parque Nacional Pico Bonito, Honduras. Phyllomedusa, 4(1): 3–16. McCranie, J.R., Wilson, L.. and Köhler, G. 2005. The amphibians & reptiles of the Bay Islands and Cayos Cochinos, Honduras. Bibliomania, Salt Lake City, UT, USA. McDiarmid, R.W., Campbell, J.A. and Toure, T.A. 1999. Snake species of the world: a taxonomic and geographic reference. Volume 1. Herpetologists’ League, Washington D.C., USA. Montgomery, C., Boback, S., Reed, R. and Frazier, J. 2015. An assessment of the impact of the pet trade on five CITES-Appendix II case studies: Cayos Cochinos Boa, Boa constrictor imperator. CITES AC28 Inf. 7. O’Shea, M. 2011. Boas and pythons of the world. New Holland, London, UK. Peters, J.. and Orejas-Miranda, B. 1986. Catalogue of the Neotropical Squamata. Part I: Snakes. 2nd Ed. Smithonian Institution Press, Washington D. C., USA. Pizzatto, L. and Marques, O. 2007. Reproductive ecology of Boine snakes with emphasis on Brazilian species and a comparison to pythons. South American Journal of Herpetology, 2(2): 107–122. Porras, L. 1999. Island Boa Constrictors (Boa constrictor). Reptiles, 7: 48–61. Price, R. and Russo, P. 1991. Revisionary comments on the genus Boa with the description of a new subspecies of Boa constrictor from Peru. The Snake, 23(1): 29–35. Quick, J., Reinert, H., de Cuba, E. and Odum, R. 2005. Recent occurrence and dietary habits of Boa constrictor on Aruba, Dutch West Indies. Journal of Herpetology, 39(2): 304–307. Reed, R., Boback, S., Montgomery, C., Green, S., Stephens, Z. and Watson, D. 2007. Ecology and conservation of an exploited insular-endemic population of Boa constrictor (Squamata: Boidae) in the Cayos Cochinos, Honduras. In: Henderson, R.., Rowell, R., Schuett, G.. and Douglas, M.. (Eds.). Biology of the boas, pythons, and related taxa. Eagle Mountain Publishing, Eagle Mountain, , USA, pp. 388–404. Reed, R.N. 2005. An ecological risk assessment of non-native boas and pythons as potentially invasive species in the United States. Risk Analysis, 25(3): 753–766. Savage, J.M. 2002. The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, Chicago and London. Snow, R., Krysko, K., Enge, K., Oberhofer, L., Warren-Bradley, A. and Wilkins, L. 2007. Introduced populations of Boa constrictor (Boidae) and Python molurus bivittatus (Pythonidae) in southern Florida. In: Henderson, R. and Powell, R. (Eds.). Biology of Boas and Pythons. Eagle Mountain Publishing, Eagle Mountain, Utah. 365–386. Vázquez-Domínguez, E. and Suárez-Atilano, M. 2012. Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictor imperator on Cozumel Island. Biological Invasions, 14: 2101–2116. WCMC, IUCN/SSC and TRAFFIC 1993. Significant trade in wildlife: a review of selected animal species in CITES Appendix II. Draft report to the CITES Animals Committee, Cambridge, UK. Wilson, L.. and Cruz Diaz, G. 1993. The herpetofauna of the Cayos Cochinos, Honduras. Herpetological Natural History, 1: 13–23. Wilson, L.D. and McCranie, J.R. 2004a. The conservation status of the herpetofauna of Honduras. Amphibian and Reptile Conservation, 3(1): 6–33. Wilson, L.D. and McCranie, J.R. 2004b. The herpetofauna of the cloud forests of Honduras. Amphibian & 31 Boa constrictor

reptile conservation, 3(1): 34–48. Wilson, L.D. and Townsend, J.H. 2007. Biogeography and conservation of the herpetofauna of the Upland Pine-Oak Forests of Honduras. Biota Neotropica, 7(1). Wilson, L.D. and Townsend, J.H. 2006. The herpetofauna of the rainforests of Honduras. Caribbean Journal of Science, 42(1): 88–113.

32 Gopherus berlandieri

TESTUDINES: TESTUDINAE Gopherus berlandieri II/B

SYNONYMS: Gopherus polyphemus berlandieri, Scaptochelys berlandieri, Testudo berlandieri, Testudo bicolor, Xerobates berlandieri

COMMON NAMES: Texas Tortoise (EN), Gophère du Texas, (FR), Tortuga de Texas (ES)

RANGE STATES: Mexico, United States

UNDER REVIEW: Mexico, United States

Current Article 4.6(b) import restriction for wild specimens from Mexico and EU DECISIONS: United States of America first applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Lower Risk/least concern (needs updating)

Trade patterns Gopherus berlandieri was listed in Appendix II on 01/07/1975 as part of the genus listing for Gopherus and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the family listing for Testudinidae.

Mexico: Mexico has not published annual export quotas for G. berlandieri for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

Direct exports of G. berlandieri from Mexico to the EU-28 2005-2014 comprised low levels of trade in live individuals, the majority of which were captive-bred (source C) or captive-produced (source F) for commercial purposes (Table 1). Direct trade in G. berlandieri from Mexico to countries other than the EU-28 2005-2014 also predominately comprised live captive-bred (C) or captive-produced (F) individuals for commercial purposes.

Indirect trade of G. berlandieri to the EU-28 originating in Mexico 2005-2014 involved very low levels of live captive-bred (source C) and captive- produced (source F) individuals, all re-exported via the United States for commercial purposes (Table 2).

33 Gopherus berlandieri

Table 1: Direct exports of Gopherus berlandieri from Mexico to the EU-28 (EU) and the rest of the world (RoW), 2005-2014. All trade was in live individuals.

Importer Purpose Source Reported by 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 EU S F Importer Exporter 11 O Importer Exporter 15 T C Importer 9 22 Exporter 9 32 15 F Importer 15 20 20 Exporter 40 40 30 Z C Importer 3 Exporter RoW P F Importer Exporter 3 I Importer 1 Exporter S F Importer Exporter 10 T C Importer 29 Exporter 12 30 F Importer Exporter 40 I Importer 8 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016. Table 2: Indirect exports of Gopherus berlandieri originating in Mexico to the EU-28, 2005-2014. All trade was in live individuals for commercial purposes. No trade was reported 2012-2014.

Source Reported by 2005 2006 2007 2008 2009 2010 2011 C Importer 5 Exporter 3 F Importer 3 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 10/03/2016.

United States: The United States has not published annual export quotas for G. berlandieri for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

There were no direct exports of G. berlandieri from the United States to the EU-28 2005-2014. Direct trade in G. berlandieri from United States to countries other than the EU-28 2005-2014 was reported in 2013 only, and consisted of two wild-sourced specimens for scientific purposes, reported by the exporter.

No indirect trade of G. berlandieri to the EU-28 originating in the United States 2005-2014 was reported. Conservation status Gopherus berlandieri is the smallest species within the genus, with a carapace length between 12 and 24 cm (Rose and Judd, 1989). G. berlandieri was reported to occur in Texas in the southern United States with a range extending into Northern Mexico (Bonin et al.,2006; Fritz and Havaš, 2007). G. berlandieri in

34 Gopherus berlandieri

southern Texas were reported to have a home range size of 3-46 ha (Kazmaier et al., 2002). The species was reported to occur in semi-desert scrub (Rose and Judd, 1989) and habitats with a “broad range of woody canopies” up to an altitude of 300 m above sea level (Rose and Judd, 2014). It was considered likely that the species also inhabits several barrier islands (Rose and Judd, 1989). It has been suggested that survival of the species in the wild is linked to the abundance of prickly pears Opuntia engelmannii, an important food and water source (Rose et al., 2011).

G. berlandieri is not adapted for burrowing, unlike other Gopherus spp. (Bonin et al. 2006). Individuals retreat under dense vegetation or construct shallow burrows, often less than 1 m deep (Bonin et al., 2006).

Hellgren et al. (2000) reported that females reach sexual maturity between four and eight years old and laid an average clutch size of approximately two eggs. Judd and Rose (2000) noted that it was common for individuals to live for 30-50 years.

In 1996, G. berlandieri was assessed as Lower Risk/least concern by the IUCN, although no information regarding the trends in population of the species was provided in the assessment and the assessment is in need of updating (Tortoise & Freshwater Turtle Specialist Group, 1996).

Threats to the species were reported to include loss of habitat resulting from agriculture and urban development, as well as mortality from road collisions (Bonin et al., 2006; Fuji and Forstner, 2010).

Judd and Rose (2000) reported that they were not aware of any systematic population monitoring or habitat management programs specifically for G. berlandieri.

Mexico: Mexico was reported to constitute over half of the geographic range of G berlandieri (Judd and Rose, 2000). The species was found to occur in north eastern Mexico in Tamaulipas, north eastern San Luis Potosí, northern and eastern Nuevo León, and Coahuila (Fritz and Havaš, 2007). Its range was reported to include the mountain ranges Sierra de Picacho, Sierra de Papagayos, Sierra de San Carlos and Sierra de Tamaulipas (Rose and Judd, 2014).

Judd and Rose (2000) and Rose and Judd (1989; 2014) reported that the status of G. berlandieri in Mexico was unknown but noted in 1989 that the densities did “not appear high” and that populations were fragmented. Within a 50 ha study area in Llera municipality, Tamaulipas, a density of two individuals per ha was recorded (Medellín Cabrera et al., n.d.)

Loss of habitat was reported as a threat to the species in Mexico (Rose and Judd, 2014). Direct killing of individuals to produce souvenirs for tourists was also noted (Rose and Judd, 1989). TRAFFIC reported that G. berlandieri had been found for sale in local markets and pet shops in Mexico (Fitzgerald et al., 2004) and the Federal Attorney for Environmental Protection (PROFEPA) reported that there was illegal trade of the species in Charco Cercado, San Luis Potosí between 1979 to 2011 (Sosa-Escalante, 2011).

The species was listed as Threatened in the NOM-059, a list issued by the Federal Government, in 1994, 2001 and 2010 (Macip-Ríos et al., 2015; SEMARNAT 2010) and it was included in the CONABIO list of priority species for conservation action in Mexico in 2012 (CONABIO, 2012). The use and development of species classified as “Theatened” in NOM-059 was reportedly permitted only with a permit issued by SEMARNAT (The Commission for Environmental Cooperation, 2003). Bonin et al. (2006) reported that the species was “theoretically protected by law” in Tamaulipas.

United States: Gopherus berlandieri was reported to occur only in the state of Texas (Judd and Rose, 2000). It was found in low hills (Bonin et al., 2006) predominately within “continuous thorn scrub savanna and woodland” (Kazmaier et al., 2001). It was reported to occur within protected areas, namely

35 Gopherus berlandieri

Laguna Atascosa National Wildlife Refuge and Welder Wildlife Refuge, both in Texas (Bonin et al., 2006).

G. berlandieri was classified as Threatened in Texas according to the Texas Administrative Code (section 65.175) (Texas Administrative Code, 2015). Hellgren et al. (2000) and Kazmaier et al., (2001) estimated the population within Chaparral Wildlife Management Area in Dimmit and LaSalle counties, Texas, with an area of 6150 ha to range between 1576 and 1751 individuals between 1994 and 1996 with density estimated to be 0.26-0.28 individuals per ha (Hellgren et al. 2000). Bonin et al. (2006) reported densities of 23 individuals per ha near Brownsville, Texas. Thode (1999) reported that the population in the Rio Grande Valley, where the central range of the species is located, had declined as a result of the loss of habitat.

Within Texas, the species was reported to the threatened by “agricultural practices and urban development” (Fuji and Forstner, 2010), mortality due to traffic collisions, direct killing by ranch workers (Rose and Judd, 1989) and entanglement in agricultural fencing (Engeman et al., 2004). A study of tortoise trade in Texas in 1999-2001 reported that G. berlandieri were exported from Texas but no individuals were found for sale in pet shops or food markets (Ceballos and Fitzgerald, 2004). Hibbits and Hibbits (2016) noted that the collection of G. berlandieri for the pet trade in the 1950s and 1960s was one for the most well-known cases of collection causing a reduction in local population of turtles in Texas.

Chapter 67 of the Texas Parks and Wildlife Code states that permits are required to take, possess, transport or offer for sale threatened non-game species (Texas Parks and Wildlife, 1997). Protection of the species was reportedly introduced in 1967 as a result of “a presumed low reproductive rate” and collection for the pet trade (Judd and Rose, 1983). However, enforcement of the law in Texas was considered to be a concern (Rose and Judd 1989; Rose and Judd, 2014) and it was reported that the species was not protected under Federal law (Rose and Judd, 2014). References Bonin, F., Devaux, B. and Dupré, A. 2006. Turtles of the world. A&C Black, London (UK). 416 pp. Ceballos, C.P. and Fitzgerald, L. a 2004. The trade in native and exotic turtles in Texas The trade in native and exotic turtles in Texas. The Wildlife Society, 32(3): 881–891. CONABIO 2012. Propuesta de lista de especies prioritarias para la conservación en México. Orozco, B.A., Bermejo, A.V., Osorio, P.K., Romo, L.C., de la Cruz Robles, E., Chávez, M.C. and del Prado Gasca, K.S. (Eds.). Engeman, R.M., Pipas, M.J. and Smith, H.T. 2004. Gopherus berlandieri (Texas tortoise). Mortality. Herpetological Review, 35(1): 54–55. Fitzgerald, L.A., Painter, C.W., Reuter, A. and Hoover, C. 2004. Collection, trade, and regulation of reptiles and amphibians of the Chihuahuan Desert ecoregion. TRAFFIC North America, Washington D.C. Fritz, U. and Havaš, P. 2007. Checklist of chelonians of the world. Vertebrate Zoology, 57(2): 148–368. Fuji, A. and Forstner, R.J. 2010. Genetic Variation and Population Structure of the Texas Tortoise, Gopherus berlandieri (Testudinidae), with Implications for Conservation. Available at: http://search.proquest.com/openview/d8b79d66b1ea7376ced3551ab12dcf87/1?pq-origsite=gscholar. [Accessed: 13/11/2015]. Hellgren, E.C., Kazmaier, R.T., Ruthven, D.C. and Synatzske, D.R. 2000. Variation in tortoise life history: demography of Gopherus berlandieri. Available at: http://ichthyology.usm.edu/courses/community/tortoise_life_history.pdf. [Accessed: 13/11/2015]. Hibbits, T.D. and Hibbits, T.L. 2016. Texas turtles and crocodilians. A field guide. 1st Edition. University of Texas Press, Austin, USA. Judd, F.W. and Rose, F.L. 2000. Conservation status of the Texas tortoise Gopherus berlandieri. Occasional Papers of the Museum of Texas Tech University, 196: 1–12. Judd, F.W. and Rose, F.L. 1983. Population structure, density and movements of the Texas tortoise Gopherus berlandieri. The Southwestern Naturalist, 28(4): 387–398. Kazmaier, R.T., Hellgren, E.C., Synatzske, D.R. and Rutledge, J.C. 2001. Mark-recapture analysis of 36 Gopherus berlandieri

Population parameters in a Texas tortoise (Gopherus berlandieri) population in Southern Texas. Journal of Herpetology, 35(3): 410–417. Kazmaier, R.T., Hellgren, E.C. and Ruthven, D.C. 2002. Home range and dispersal of Texas tortoises, Gopherus berlandieri, in a managed thornscrub ecosystem. Chelonian Conservation and Biology, 4(2): 488–496. Macip-Ríos, R., Ontiveros, R., López-Alcaide, S. and Casas-Andreu, G. 2015. The conservation status of the freshwater and terrestrial turtles of Mexico: a critical review of biodiversity conservation strategies. Revista Mexicana de Biodiversidad, 86: 1048–1057. Medellín Cabrera, A., Martínex-Hinojosa, A.I. and Cumpián Meddellín, J.I. n.d. Conservacion y aprovechamiento ecoturistico de la tortuga terrestre Gopherus berlandieri en Llera, Tamaulipas. Avaialable at: http://www.uaemex.mx/Red_Ambientales/docs/memorias/Resumen/EA/RC/EAC- 03.pdf [Accessed 14/03/2016]. Rose, F.L. and Judd, F.W. 1989. Gopherus berlandieri Berlandier’s Tortoise, Texas Tortoise. In: Swingland, I.R., Klemens, M.W., IUCN/SSC Tortoise and Freshwater and The Durrell Institute of Conservation and Ecology (Eds.). The conservation biology of tortoises. 8–9. Available at: https://books.google.co.uk/books?id=pL2vyHjC4akC&pg=PA136&dq=texas+%22Gopherus+berland ieri%22&hl=en&sa=X&ved=0CDkQ6AEwBmoVChMI3enZkLqNyQIVB2kUCh1fDgdo#v=snippet&q= Gopherus berlandieri&f=false. Rose, F.L. and Judd, F.W. 2014. The Texas Tortoise: A Natural History Vol. 13. Norman, Oaklahoma, University of Oklahoma Press, USA. Rose, F.L., Judd, F.W. and Small, M.F. 2011. Survivorship in Two Coastal Populations of Gopherus berlandier. 45(1): 75–78. SEMARNAT 2010. NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental- Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. DIARIO OFICIAL, 1: 1–78. Sosa-Escalante, J.E. 2011. Aplicación de la Ley para el Combate del Tráfico Ilegal de Vida Silvestre en México: El caso de Charco Cercado. THERYA, 2(3): 245–262. Texas Administraive Code 2015. Threatened Species. Section 65.175 of Title 31 of the Texas Administrative Code. Available at: http://texreg.sos.state.tx.us/public/readtac$ext.ViewTAC?tac_view=5&ti=31&pt=2&ch=65&sch=G&r l=Y. [Accessed: 14/03/2016]. Texas Parks and Wildlife 1997. Parks and Wildlife Code, Title 5. Wildlife and conservatio Subtitle B. hunting and fishing. Chapter 67 Non game species. Available at: http://www.statutes.legis.state.tx.us/Docs/PW/htm/PW.67.htm. [Accessed: 15/03/2016]. Thode, B.R. 1999. The Effects of Human Presence on the Texas Tortoise (Gopherus berlandieri) in Southern Texas and Northern Mexico. Cantaurus, 7: 41–43. The Commission for Environmental Cooperation 2003. Summary of Environmental Law in Mexico. Available at: https://moose.cec.org/moose/lawdatabase/mxdoc.cfm?varlan=english&topic=17. [Accessed: 15/03/2016]. Tortoise & Freshwater Turtle Specialist Group 1996. Gopherus berlandieri. Available at: http://www.iucnredlist.org/details/9401/0. [Accessed: 13/11/2015].

37 Galanthus nivalis

LILIALES: Galanthus nivalis II/B

SYNONYMS Chianthemum nivale, Galanthus atkinsii hort. Barr, Galanthus imperati, Galanthus montana, Galanthus nivalis humboldtii, Galanthus nivalis imperati, Galanthus nivalis subplicatus, Galanthus plicatus sens. Guss., Galanthus plicatus subplicatus, Galanthus reflexus auct. non Herb. ex Lindl., Galanthus sharlokii, Galanthus shaylockii (sic)

COMMON NAMES: Common Snowdrop (EN), Galantine d'Hiver (FR), Campanilla de invierno (ES)

RANGE STATES: , , Belgium (introduced), , , , Former USSR, , Germany, , , (introduced), (introduced), , Republic of , Russian Federation, , Spain (distribution uncertain), (introduced), Switzerland, Turkey, , of and Northern (introduced)

UNDER REVIEW: Bosnia and Herzegovina, Switzerland, Ukraine

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Bosnia and Herzegovina, Switzerland and Ukraine first applied on 29/10/2001 and last confirmed on 28/05/2015. Previous negative opinion for Bosnia and Herzegovina, Switzerland and Ukraine applied 02/09/1997 and previous no opinion ii) for Bosnia and Herzegovina, Switzerland and Ukraine applied on 22/07/1997.

Current no opinion ii) for wild specimens from Albania, Norway, Republic of Moldova, Russian Federation and Turkey first applied 22/07/1997.

IUCN: Near Threatened

Trade patterns Galanthus nivalis was listed in Appendix II on 18/01/1990 and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the genus listing for Galanthus.

Bosnia and Herzegovina: Bosnia and Herzegovina joined CITES on 21/01/2009 and accession entered into force on 21/04/2009. The country has not published annual export quotas for G. nivalis for the period 2005-2016. Bosnia and Herzegovina reported ‘no trade’ 2010-2012 and has submitted annual reports for 2013 and 2014.

No direct exports of G. nivalis from Bosnia and Herzegovina to the EU-28 or countries other than the EU-28 were reported for the period 2005-2014. No indirect trade in G. nivalis originating in Bosnia and Herzegovina to the EU-28 was reported 2005-2014.

Switzerland: Switzerland has not published annual export quotas for G. nivalis for the period 2005-2016 and has submitted annual reports for all years 2005-2013; Switzerland has not yet submitted an annual report for 2014.

38 Galanthus nivalis

No direct exports of G. nivalis from Switzerland to the EU-28 or countries other than the EU-28 were reported for the period 2005-2014. No indirect trade in G. nivalis originating in Switzerland to the EU-28 was reported 2005-2014.

Ukraine: Ukraine has not published annual export quotas for G. nivalis for the period 2005-2016. Ukraine has submitted annual reports for all years 2005-2013; Ukraine has not yet submitted an annual report for 2014.

No direct exports of G. nivalis from Ukraine to the EU-28 or countries other than the EU-28 were reported for the period 2005-2014. No indirect trade in G. nivalis originating in Ukraine to the EU-28 was reported 2005-2014. Conservation status Galanthus nivalis is a bulbous plant that produces a white (Berkov et al., 2012; Crook and Davis, 2013) and is commonly cultivated for horticultural trade (Crook and Davis, 2013).

The distribution of the species was reported to range “eastwards from the Pyrenees and northern Spain to the Ukraine and southwards from Germany and Poland to southern Italy, Albania and Northern Greece” (Crook and Davis, 2013). It was reported that most populations were below an altitude of 900 m but that the upper elevation limit was 2314 m (Crook and Davis, 2013). The habitat of G. nivalis was reported to include deciduous woodland (Grey-Wilson and Matthew, 1981; Crook and Davis, 2013) and occassionally coniferous forest, as well as meadows, pastures and scrub (Crook and Davis, 2013).

G. nivalis was assessed as Near Threatened by the IUCN and it was reported that the species may qualify for a threat category in the near future as the population was decreasing (Crook and Davis, 2013). Crook and Davis (2013) added that the species was listed in “nearly every country’s Red List”, from which they suggested the subpopulation in each country was threatened.

G. nivalis was reported to be threatened by loss of habitat, climate change, harvesting and trade (Crook and Davis, 2013). However, Bishop et al. (2001) reported that given the control and monitoring of trade through CITES, trade was unlikely to endanger wild populations of Galanthus. The species was listed on the European Annex V (Bilz et al., 2011) which lists “animal and plant species of community interest whose taking in the wild and exploitations may be subject to management measures” (Council of the European Communities, 1992).

Bosnia and Herzegovina: G. nivalis was reported to occur in Kozara and Osječenica in the north west, Ozren in the north east, Raduša in the west, Vlašić, Vranica, Trebević and Bitovnja in central Bosnia Herzegovinia, Mostara in the south west and Trebinja in the south (Greenway, 2013).

Within the two constitutional regions within the country, the species was assessed as Least Concern in the 2013 Red List of the Federation of Bosnia and Herzegovina administrative region (Greenway, 2013), but it was not included in the 2013 Red List of the Republika Srpska administrative region (Republika Srpska, 2013). Prior to this, G. nivalis was assessed as Vulnerable in Bosnia and Herzegovina in 1996 (Šilić, 1996 in in Crook and Davis, 2013). Galanthus nivalis was previously protected against picking, collecting, uprooting, destruction, possession or trade by Article 35 of the Law on Nature Protection (2003) which applied to all plants on the Red List, including all species assessed as Vulnerable. However, this law was repealed in 2013 and was replaced by the Bosnia and Herzegovnia: Law on Nature Protection (2013) which only restricts these activities for “strictly protected species” and, therefore, does not apply to G. nivalis.

The Bosnia and Herzegovina CITES Management Authority reported that they have no records of illegal trade of G. nivalis (Medić, pers. comm to UNEP-WCMC, 2015).

39 Galanthus nivalis

Switzerland: G. nivalis was reported to occur in the northern half of Switzerland as well as in the southern point of Ticino, in the south of the country (The National Data and Information Center of the Swiss Flora, 2013).

G. nivalis was assessed as Near Threatened in Switzerland, as well as being classed as Near Threatened in the regions of Jura [north western Switzerland], Mitteland [north central Switzerland], the Northern Alps, the Southern Alps, and it was assessed as Vulnerable in the Eastern Central Alps (Moser et al., 2002). No estimates of population size in Switzerland were found.

The level of protection for the species was reported to vary between regions including “full protection” in Aargau, Basel-Country, Nidwalden, Solothurn and Ticino and “partial protection” in Bern, Neuenberg and St Gallen (The National Data and Information Center of the Swiss Flora, 2013). Full protection prohibits digging up, selling, and purchase of the species without a permit (de Klemm, 1997). Partial protection reportedly prohibits the collection of plants for commercial purposes without a permit, the uprooting of plants and limits picking of aerial parts of the plant to limited numbers, often defined as a small bunch (de Klemm and Shine, 1993), although in St Gallen and Bern, no more than five inflorescences may be picked (Naturschutzverordnung, 2007; de Klemm, 1997). In all regions, the collection of all species of wild plants for commercial purposes was reported to require authorisation from the cantonal authority, according to Article 19 of the federal law on natural and cultural heritage in Switzerland (de Klemm, 1997; Bundesgesetzüber den Natur- und Heimatschutz, 1966).

Ukraine: G. nivalis was reported to be previously widely distributed in the East Carpathians, but its range was reduced in the 1970s and 1980s as a result of loss of habitat, and the collection of and (Budnikov and Kricsfalusy, 1994; Crook and Davis, 2013). Within Transcarpathia, in western Ukraine, G. nivalis was reported to occur in small patches from an altitude of 100 m, into the East Carpanthians up to an altitude of 1500 m (Budnikov and Kricsfalusy, 1994).

Domashlinets (in. litt. to UNEP-WCMC, 2015) reported that G. nivalis was listed in the Red Data Book of Ukraine but was not given a specific threat category. The 2009 edition of which described populations of G. nivalis in Ukraine as “heavily decreasing” (Didukh, 2010). G. nivalis was reported as “rare” in Ukraine (Montemaggiori et al., 2005). The species was also listed in the 1996 “Red Data Book of the Ukraine” as a species in decline and included in the “List of Rare and Disappearing Species of Ukrainian Flora” in 1996 (Crook and Davis, 2013).

The Economic Comimission for Europe (1999) noted that 10 000 ha had been protected in Ukraine to preserve medicinal plants including G. nivalis. Unauthorised collection of G. nivalis from the wild was reported to be prohibited, although collection from protected areas has been reported (Domashlinets, 2015). The trade in medicinal and ornamental plant species and their parts is prohibted (Article 9, no 591-XIV- Supreme Council of Ukraine, 1999). It was also noted to be illegal to purchase or sell, destroy the habitats of, or remove from the wild any plants listed in the Red Book of Ukraine (The State Ecological Inspectorate in Luhansk region, 2015). Illegal trade in G. nivalis from Ukraine was reported in 1997 (Crook and Davis, 2013). References Berkov, S., Codina, C. and Bastida, J. 2012a. The Genus Galanthus : A Source of Bioactive Compounds. In: Rao, V. (Ed.). Phytochemicals - A global perspective role in nutritional and health. InTech, Rijeka, & Shanghai, China. 235–254. Bilz, M., Kell, S.P., Maxted, N. and Lansdown, R.V. 2011. European Red List of Vascular Plants. Luxembourg. Bishop, M., Davis, A.P. and Grimshaw, J. 2001. Snowdrops. The Griffin Press, UK. 1-363 pp. Bosnia and Herzegovina: Law on Nature Protection 2003. Bosnia and Herzegovina: Law on Nature Protection. Available at: http://faolex.fao.org/cgi- 40 Galanthus nivalis

bin/faolex.exe?rec_id=134760&database=faolex&search_type=link&table=result&lang=eng&format_ name=@ERALL. [Accessed: 18/02/2016]. Bosnia and Herzegovnia: Law on Nature Protection 2013. Bosnia and Herzegovina: Law on Nature Protection 2013. Zakon o zaštiti prirode FBiH. Available at: http://faolex.fao.org/cgi- bin/faolex.exe?rec_id=143206&database=faolex&search_type=link&table=result&lang=eng&format_ name=@ERALL. [Accessed: 18/02/2016]. Budnikov, G. and Kricsfalusy, V. 1994. Bioecological study of Galanthus nivalis L. in the east Carpathians. Thaiszia Journal of Botany. Košice, 4: 49–75. Bundesgesetzüber den Natur- und Heimatschutz 1966. Systematische Sammlung des Bundesrechts (SR) 451. Available at: https://www.admin.ch/opc/de/classified-compilation/19660144/index.html. [Accessed: 27/11/2015]. Council of the European Communities 1992. Council directive 92/43/EEC on the conservation of natural habitats and of wild fauna and flora (Habitats Directive). Official Journal of the European Communities, L 206/7. Crook, V. and Davis, A. 2013. Galanthus nivalis. Available at: http://www.iucnredlist.org/details/162168/0. [Accessed: 2/11/2015]. Didukh, Y.P. 2010. ‘Red Data Book of Ukraine. Vegetable Kingdom’ Afterword. Biodiversity: Research and Conservation, 19: 87–92. Domashlinets, V. 2015. Volodymyr Domashlinets (information from M.G. Holodny Institute of Botany of the National Academy of Sciences of Ukraine) of CITES Management Authority of Ukraine in litt. to UNEP-WCMC 18/12/2015. Economic Comimission for Europe 1999. UN. Environmental Performance Review Series No. 6. Ukraine. Available at: http://www.unece.org/fileadmin/DAM/env/epr/epr_studies/ukraine.pdf. [Accessed: 27/11/2015]. Greenway 2013. Red list of flora of the Federation of Bosnia and Herzegovina. Crvena lista flore Federacije Bosne i Hercegovine. Sarajevo. Grey-Wilson, C. and Matthew, B. 1981. Bulbs. The bulbous plants of Europe and their allies. William Collins Sons & Co Ltd, London. de Klemm, C. 1997. Comparative analysis of the effectiveness of legislation for the protection of wild flora in Europe. Nature and environment No. 88. Council of Europe Publishing. de Klemm, C. and Shine, C. 1993. Biological diversity conservation and the law: legal mechanisms for conserving species and ecosystems. IUCN Environmental Policy and Law paper no. 29. IUCN, Gland, Switzerland and Cambridge, UK. Medić V. 2015. Vanda Medić (Bosnia and Herzegovina CITES management authority) pers. comm to UNEP-WCMC 11/12/2015. Montemaggiori, A., Capula, M., Gippoliti, S., Marsden, S.J., Mertens, A., Rondinini, C., Salerno, G. and Sorace, A. 2005. A study of species which are subject to import restrictions according to the article 4.6 of Regulation 338/97. Istituto Ecologia Applicata. Moser, D., Gygax, A., Bäumler, B., Wyler, N. and Palese, R. 2002. Red List of the Threatened Ferns and Flowering Plants of Switzerland (Rote Liste der gefährdeten Farn- und Blütenpflanzen der Schweiz). Bundesamt für Umwelt, Wald und Landschaft, Bern; Zentrum des Datenverbundnetzes der Schweizer Flora, Chambésy; Conserva. Naturschutzverordnung 2007. Verordnung über den Schutz wildwachsender Pflanzen und freilebender Tiere (Naturschutzverordnung) (NSV). Available at: http://www.gesetzessammlung.sg.ch/frontend/versions/1233. [Accessed 14/03/2016] Republika Srpska 2013. Red list of protected species of flora and fauna. Republica Srpska. Available at: http://nasljedje.org/docs/crvenalista/Lista_vaskularne_flore.pdf. [Accessed 14/03/2016 Šilić, Č. 1996. The List of Plant Species (Pteridophyta and Spermatophyta) for the Red Book of Bosnia and Herzegovina. Glasnik Zemaljskog Muzeja Bosne i Hercegovine, Sarajevo. Supreme Council of Ukraine 1999. With law decree of Ukraine. On Flora 591-14. Available at: http://zakon1.rada.gov.ua/laws/show/591-14. [Accessed: 6/11/2015]. The National Data and Information Center of the Swiss Flora 2013. Galanthus nivalis. Available at: https://www.infoflora.ch/de/flora/3128-galanthus-nivalis.html. [Accessed: 6/11/2015]. The State Ecological Inspectorate in Luhansk region 2015. Державна екологічна інспекція у Луганській областіДержавний нагляд у сфері охорони навколишнього природного середовища ‘Первоцвіт’. Available at: http://deilg.gov.ua/actions/pervocvit/. [Accessed: 6/11/2015]. 41 Orchis mascula

ORCHIDALES: ORCHIDACEAE Orchis mascula II/B

COMMON NAMES: Early Purple Orchid (EN), Orchis mâle (FR)

RANGE STATES: Albania, Croatia, Czech Republic, Denmark, Estonia, Finland, Hungary, Isle of Man (United Kingdom), Latvia, Lithuania, Netherlands, Norway, Poland, Russian Federation, Sweden, Switzerland, Turkey, Ukraine, United Kingdom of Great Britain and Northern Ireland UNDER REVIEW: Albania

EU DECISIONS: Current Article 4.6(b) suspension for wild and ranched specimens from Albania first applied on 29/10/2001 and last confirmed on 28/05/2015.

IUCN: Not Assessed

Trade patterns Orchis mascula was listed in Appendix II on 01/07/1975 and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the family listing for Orchidaceae. Albania has not yet submitted annual reports for 2013 and 2014 and has not published annual export quotas for O. mascula for the period 2005-2014.

No direct or indirect trade in O. mascula from Albania to the EU-28 or countries other than the EU-28 was reported over the period 2005-2014. Conservation status Orchis mascula has a wide distribution, including Central, Southern and Eastern Europe (Williams et al., 1978; Davies et al., 1983), North Africa and the Middle East (la Croix, 2008).

O. mascula has been reported as favouring open woodland, moist pasture and thickets (Williams et al., 1978; Davies et al., 1983; la Croix, 2008) and is absent from very acidic or wet sites (Jacquemyn et al., 2009b). The species has been reported as flowering mid-spring to mid-summer (Martin, 1982; Stewart, 1995; la Croix, 2008; Jacquemyn et al., 2009b).

The species has not been assessed for the IUCN Red List (IUCN, 2015) but it was assessed as Least Concern in the European Red List of Vascular Plants (Bilz et al., 2011).

Declines of the species in Europe have been linked to a reduction in the use of traditional coppicing methods (Jacquemyn et al., 2009b). Reduction in coppicing has been linked to reduced genetic diversity of the species (Jacquemyn et al., 2009a), and reduction in mowing/grazing has been linked to overshadowing of O. mascula by shrubs and trees (Biereżnoj, 2012). Small population sizes have also been shown to negatively affect reproductive success (Meekers and Honnay, 2011).

Albania: O. mascula has been recorded as occurring in Albania (Republic of Albania Ministry Environment, Forests and Water Administration, 2013; Imami et al., 2015). It has been reported in Tomorri National Park, south central Albania (Mahmutaj et al., 2014) and around Mount Korab in the east (Pieroni et al., 2014). No further information on the population distribution, size or status in Albania could be identified.

42 Orchis mascula

All 16 Orchis spp. (with the exception of O. provincialis) are listed as Vulnerable under the Albanian National Red List Assessment (Republic of Albania Ministry Environment, Forests and Water Administration, 2013).

Orchis mascula has been reported to be harvested as a medicinal and aromatic plant in Albania and for the production of a traditional beverage, salep (Imami et al., 2015; Kreziou et al., 2015); Mahmutaj et al. (2013) reported it as one of the most collected plants for trade in Tomori National Park, Albania. Lange (pers. comm. in Kathe et al., 2003) reported that O. mascula may be exported from Albania as Orchis morio. Orchis spp. populations were reported to have been depleted due to overharvesting on the Albanian side of Mt. Korab (Pieroni et al., 2014). It has been reported that approximately 95 per cent of wild collected medicinal and aromatic plants (including Orchis spp.) were exported (Lange, 1998; Vaso 1997 in Kathe et al., 2003).

Inclusion in the Albanian National Red List appears to preclude harvesting in Albania (Albania Ministry of the Environment, 2014). Environmental licences are required for exploitation of plants (Law on Environmental Protections, No. 7664), while harvesting of non-timber forest products (including medicinal and aromatic plants) is covered under the Law on Forests and the Forest Service Police (No. 7623) and allows harvesting only after a valid permit has been obtained.

References Albania Ministry of the Environment 2014. Fifth national report of Albania to the United Nations Convention on Biological Diversity. Tirana, Albania. 49 pp. Bateman, R.M., Hollingsworth, P.M., Preston, J., Yi-Bo, L., Pridgeon, A.M. and Chase, M.W. 2003. Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society, 142: 1–40. Biereżnoj, U. 2012. A new occurrence site of Orchis mascula in the town of Suwałki (NE Poland). Chrońmy Przyrodę Ojczystą, 68(6): 448–454. Bilz, M., Kell, S.P., Maxted, N. and Lansdown, R.V. 2011. European Red List of Vascular Plants. Luxembourg. la Croix, I. 2008. The new encyclopedia of orchids: 1500 species in cultivation. Timber Press, Inc., Portland and London. 524 pp. Davies, P., Davies, J. and Huxley, A. 1983. Wild Orchids of Britain and Europe. Chatto & Windus, London. 256 pp. Duperrex, A. 1961. Orchids of Europe. Blandford Press Ltd., London, UK. 235 pp. Imami, D., Ibraliu, A., Fasllia, N., Gruda, N. and Skreli, E. 2015. Analysis of the Medicinal and Aromatic Plants Value Chain in Albania. Gesunde Pflanzen, 67: 155–164. IUCN 2015. The IUCN Red List of Threatened Species. Version 2015-4. Available at: http://www.iucnredlist.org. [Accessed: 17/11/2015]. Jacquemyn, H., Brys, R., Adriaens, D., Honnay, O. and Roldán-Ruiz, I. 2009a. Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula. Conservation Genetics, 10: 161–168. Jacquemyn, H., Brys, R., Honnay, O. and Hutchings, M.J. 2009b. Biological Flora of the British Isles: Orchis mascula. Journal of Ecology, 97: 360–377. Kathe, W., Honnef, S. and Heym, A. 2003. Medicinal and Aromatic Plants in Albania, Bosnia- Herzegovina, Bulgaria, Croatia and Romania. Bonn, Germany. 201 pp. Kreziou, A., de Boer, H. and Gravendeel, B. 2015. Harvesting of salep orchids in north-western Greece continues to threaten natural populations. Oryx, (May): 1–4. Lange, D. 1998. Europe’s medicinal and aromatic plants: their use, trade and conservation. TRAFFIC, Cambridge, UK. 119 pp. Mahmutaj, E., Merja, Y. and Hoda, P. 2013. Preliminary data on floristic richness of species with economical values in Tomorri National Park (Albania). Natura Montenegrina, 12(3-4): 657–672. Mahmutaj, E., Merja, Y. and Hoda, P. 2013. Preliminary data on floristic richness of species with economical values in Tomorri National Park (Albania). Natura Montenegrina, 12(3-4): 657–672. Martin, W.K. 1982. The New Concise British Flora. Michael Joseph Limited & Ebury Press, London, UK. 43 Orchis mascula

247 pp. Meekers, T. and Honnay, O. 2011. Effects of habitat fragmentation on the reproductive success of the nectar-producing orchid Gymnadenia conopsea and the nectarless Orchis mascula. Plant Ecology, 212(11): 1791–1801. Pieroni, A., Nedelcheva, A., Hajdari, A., Mustafa, B., Scaltriti, B., Cianfaglione, K. and Quave, C.L. 2014. Local knowledge on plants and domestic remedies in the mountain villages of Peshkopia (Eastern Albania). Journal of Mountain Science, 11(1): 180–193. Republic of Albania Ministry Environment Forests and Water Administration 2013. Red List of Wild Flora and Fauna, Albania. 28 pp. Stewart, J. 1995. Manual of Orchids - the new Royal Horticultural Society dictionary. MacMillan Reference Books, London, UK. Williams, J.G., Williams, A. and Arlott, N. 1978. A Field Guide to the Orchids of Britain and Europe. Collins, London. 176 pp.

44 Cyclamen mirabile

PRIMULALES: Cyclamen mirabile II/B

RANGE STATES: Turkey

UNDER REVIEW: Turkey

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Turkey first applied on 29/10/2001 and last confirmed on 28/05/2015

IUCN: Not assessed

Trade patterns Cyclamen mirabile was listed in Appendix II on 01/07/1975 as part of the genus listing for Cyclamen and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997, also as part of a genus listing.

Turkey has not published annual export quotas for C. mirabile for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

No direct or indirect trade in C. mirabile from Turkey to the EU-28 or the rest of the world was reported over the period 2005-2014. Conservation status C. mirabile is a range-restricted perennial herb (Yesson and Culham, 2011), endemic to Turkey (Dusen et al., 2015). This species was thought to have become extinct by the middle of the 20th century due to over- harvesting, until it was rediscovered in western Turkey (Byfield, 1993). The distribution centres around south-western Turkey (Yesson and Culham, 2006; Dusen et al., 2015), and the range size was estimated as 15 321 km2 (Yesson and Culham, 2006). Historic reports placed it as most abundant in the Turkish provinces of Muğla, Aydin and Isparta (Meikle, 1978 in Dunsen et al. 2015), with more recent site-specific studies finding it around the town of Akçaova in Aydin (Dusen et al., 2015) and on the slopes of Madran Babadağ (Yamaner and Erdag, 2008).

C. mirabile flowers between September and November (Debussche et al., 2004; Dusen et al., 2015), and seeds are reportedly released during late May the following year (Debussche et al., 2004; Yesson and Culham, 2006). Surveys showed it to favour organic, rich soils in oak and pine woodland at altitudes ranging from 500 to 1000 m (Dusen et al., 2015).

This species has not yet been assessed by the IUCN, but the Red Book of Turkish plants (Ekim et al., 2000) classified it as Endangered based on the IUCN Red List criteria. It was described as rare by Yesson and Culham (2011). A more recent assessment by Dusen et al. (2015) also classified this species as Endangered due to “grazing, tourism, industrialization and urbanization” threats causing population declines, whilst Ciotir et al. (2008) classified it as Critically Endangered based on an estimated decrease in range size of more than 80 per cent by 2050.

Historically, the main threat to the species has been the harvesting of wild bulbs of other similar species (Read, 1989; Jenkins and Oldfield, 1992), which cannot be specifically identified until flowering, meaning that wild tubers were likely exported in shipments of other, more common species (Jenkins and Oldfield, 1992). Although there appeared to be little information about levels of illegal harvesting, a 45 Cyclamen mirabile

TRAFFIC report noted that seizures of illegal Cyclamen continued to be reported (Kecse-nagy et al.,2006). The species was also considered to be at risk from climate change due to its restricted altitudinal range: based on future climate scenarios, a range loss of 20 - 100 per cent was predicted for this species by 2050 (Yesson and Culham, 2006; Yesson et al., 2009).

A ban on the export of all wild endemic Cyclamen is reportedly in place, although this was considered difficult to enforce (Kecse-nagy et al., 2006). No further information on the management of C. mirabile in Turkey was found. This species is, however, readily cultivated (Grey-Wilson, 2002), and can be artificially propagated (Yamaner and Erdag, 2008), which may reduce, though not alleviate the demand for wild-sourced specimens (Kecse-nagy et al., 2006). References Byfield, A. 1993. Indigenous propagation project, Turkey. Oryx, 27(1): 65–67. Ciotir, C., Yesson, C. and Culham, A. 2008. Future predictions of Cyclamen distribution in the Mediterranean region. Available at: http://dx.doi.org/10.1038/npre.2009.3066.1. [Accessed: 3/12/2015]. Debussche, M., Garnier, E. and Thompson, J.D. 2004. Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen. Botanical Journal of the Linnean Society, 145(4): 469–484. Dusen, O.D., Gurcan, B. and Mammadov, R. 2015. Morphology, Anatomy and Palynology of endemic Cyclamen mirabile hildebr. (Primulaceae) in South-West Turkey. Bangladesh Journal of Botany, 43(3): 243–247. Ekim, T., Koyuncu, M., Vural, M., Duman, H., Aytaç, Z. and Digüzel, N. 2000. Türkiye Bitkileri Kirmizi Kitabi (Egrelti ve Tohumlu Bitkiler) [Red Data Book of Turkish Plants (Pteridophyta and Spermatophyta)]. Ankara. 1–246 pp. Grey-Wilson, C. 2002. Cyclamen: a guide for gardeners, horticulturists and botanists. 2nd Ed. Pavilion Books Company Ltd, London, UK. Jenkins, M. and Oldfield, S. 1992. Wild plants in trade. TRAFFIC International, Cambridge, UK. Kecse-nagy, K., Papp, D., Knapp, A. and Meibom, S.V.O.N. 2006. Wildlife Trade in Central and Eastern Europe: A Review of CITES Implementation in 15 Countries. TRAFFIC Europe report, Budapest, Hungary. Meikle, R.. 1978. Cyclamen L. In: Davis, P.. (Ed.). Flora of Turkey and the East Aegean Islands, Vol. 6. Edinburgh University Press, Edinburgh, U.K. 128–135. Read, M. 1989. The trade - a threat to wild plant populations. Oryx, 23(3): 127–134. Yamaner, O. and Erdag, D. 2008. Direct shoot formation and microtuberization from aseptic seedlings of Cyclamen mirabile Hildebr. Biotechnology, 7(2): 328–332. Yesson, C. and Culham, A. 2006. A phyloclimatic study of Cyclamen. BMC Evolutionary Biology, 6(1): 72. Yesson, C. and Culham, A. 2011. Biogeography of Cyclamen: an application of phyloclimatic modelling. In: Hodkinson, T., Jones, M., Waldren, S. and Parnell, J. (Eds.). Climate Change, Ecology and Systematics. Cambridge University Press, Cambridge (UK). 265–279. Yesson, C., Toomey, N.H. and Culham, A. 2009. Cyclamen: time, sea and speciation biogeography using a temporally calibrated phylogeny. Journal of Biogeography, 36(7): 1234–1252.

46 Cyclamen pseudibericum

PRIMULALES: PRIMULACEAE

Cyclamen pseudibericum II/B

RANGE STATES: Turkey

UNDER REVIEW: Turkey

EU DECISIONS: Current Article 4.6(b) suspension for wild imports from Turkey first applied on 29/10/2001 and last confirmed on 28/05/2015.

IUCN: Not assessed

Trade patterns Cyclamen pseudibericum was listed in Appendix II on 01/07/1975 as part of the genus listing for Cyclamen and was included in Annex B of the EU Wildlife Trade Regulations on 01/06/1997, also as part of a genus listing.

Turkey has not published annual export quotas for C. pseudibericum for the period 2005-2016 and has submitted annual reports for all years 2005-2014.

No direct or indirect trade in C. pseudibericum from Turkey to the EU-28 or the rest of the world was reported over the period 2005-2014. Conservation status C. pseudibericum is a range-restricted perennial herb endemic to Turkey (Anderberg, 1994; Curuk et al., 2015). It is found in moist, mountainous areas around the north-eastern Mediterranean sea (Grey- Wilson, 2002; Yesson and Culham, 2006). Surveys showed it to favour oak/pine woodland and shrubland at altitudes ranging from 800 to 1320 m (Celemli et al., 2015; Curuk et al., 2015).

C. pseudibericum was estimated to have a range size of 14 767 km2 (Yesson and Culham, 2006), and a distribution centring around the northern Amanus (Nur) and the southern Anti-Taurus mountain ranges in south-central Turkey, primarily in Adana, Osmaniye and Hatay provinces (Grey-Wilson, 2002). Specifically, Çelemli et al. (2015) recorded this species as being present at the Zorkun Plateau in the Osmaniye region of the Amanos Mountains.

The species flowers during February-March (Debussche et al., 2004; Curuk et al., 2015), and seeds are reportedly released during a single week in late June (Debussche et al., 2004).

This species has not yet been assessed by the IUCN, but the Red Book of Turkish plants (Ekim et al., 2000) classified it as Endangered based on the IUCN Red List criteria. A more recent assessment by Ciotir et al. (2008) classified it as Critically Endangered based on an estimated decrease in range size of more than 80 per cent by 2050. Although there appeared to be little information about levels of illegal harvesting, a TRAFFIC report noted that seizures of illegal Cyclamen continued to be reported (Kecse- nagy et al.,2006). In addition to the threat from illegal trade, the species was also considered at risk from climate change due to its restricted altitudinal range: based on future climate scenarios, a range loss of up to 92 per cent was estimated for this species by 2050 (Yesson and Culham, 2006).

A ban on the export of all wild endemic Cyclamen is reportedly in place, although this was considered difficult to enforce (Kecse-nagy et al., 2006). No further information on the management of 47 Cyclamen pseudibericum

C. pseudibericum in Turkey was found. This species is, however, readily cultivated (Grey-Wilson, 2002), which may reduce, though not alleviate the demand for wild-sourced specimens (Kecse-nagy et al., 2006). References Anderberg, A. 1994. Phylogeny and subgeneric classification of Cyclamen L. (Primulaceae). Kew Bulletin, 49(3): 455–467. Celemli, O., Temizer, I. and Altinozlu, H. 2015. Anatomy, palynology of endemic Cyclamen pseudibericum in Mediterranean phytogeographic region of Turkey and chemical analysis of its tuber extracts. Hacettepe Journal of Biology and Chemistry, 43(2): 105–113. Ciotir, C., Yesson, C. and Culham, A. 2008. Future predictions of Cyclamen distribution in the Mediterranean region. Available at: http://dx.doi.org/10.1038/npre.2009.3066.1. [Accessed: 3/12/2015]. Curuk, P., Sogut, Z., Bozdogan, E., Izgu, T., Sevindik, B., Mohammad Tagipur, E., Teixeira da Silva, J.A., Serce, S., Aka Kacar, Y. and Yalcin Mendi, Y. 2015. Morphological characterization of Cyclamen sp. grown naturally in Turkey: Part I. South African Journal of Botany, 100: 7–15. Debussche, M., Garnier, E. and Thompson, J.D. 2004. Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen. Botanical Journal of the Linnean Society, 145(4): 469–484. Ekim, T., Koyuncu, M., Vural, M., Duman, H., Aytaç, Z. and Digüzel, N. 2000. Türkiye Bitkileri Kirmizi Kitabi (Egrelti ve Tohumlu Bitkiler) [Red Data Book of Turkish Plants (Pteridophyta and Spermatophyta)]. Ankara. 1–246 pp. Grey-Wilson, C. 2002. Cyclamen: a guide for gardeners, horticulturists and botanists. 2nd Ed. Pavilion Books Company Ltd, London, UK. Kecse-nagy, K., Papp, D., Knapp, A. and Meibom, S.V.O.N. 2006. Wildlife Trade in Central and Eastern Europe: A Review of CITES Implementation in 15 Countries. TRAFFIC Europe report, Budapest, Hungary. Yesson, C. and Culham, A. 2006. A phyloclimatic study of Cyclamen. BMC Evolutionary Biology, 6(1): 72.

48 Appendix

Appendix 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

49