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UNEP-WCMC technical report

Review of selected on the basis of the Analysis of 2014 CITES export quotas

Part I

(Version edited for public release)

2 Review of species selected on the basis of the Analysis of 2014 export quotas.

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

Published August 201 4

Copyright European Commission 2014

Citation UNEP-WCMC. 2014. Review of species selected on the basis of the Analysis of 2014 export quotas . UNEP-WCMC, Cambridge.

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

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Introduction and summary ...... 4 spp.: Overview of status, management and trade ...... 6 Brookesia betschi ...... 8 ...... 10 Brookesia griveaudi ...... 12 ...... 14 Brookesia nasus ...... 16 Brookesia peyrierasi ...... 18 Brookesia therezieni ...... 20 References ...... 22 Calumma parsonii ...... 26 rivularis ...... 30 Appendix ...... 34

Brookesia overview

Introduction and summary 4

This report presents a review of nine species selected on the basis of the quota analysis and provides an update of new and increased 2014 CITES export quotas published since the production of the Analysis of 2014 CITES export quotas (UNEP-WCMC, 2014).

National export quotas for CITES listed taxa are an important tool to manage and monitor wildlife trade. The establishment or revision of an export quota should be based on a non-detriment finding (NDF) by the Scientific Authority of the exporting country and the NDF should be reviewed annually (Resolution Conf. 14.7 (Rev. CoP15)). Once such annual quotas are established, the need for a NDF for each individual shipment of the species concerned is eliminated.

The EU, through stricter measures outlined in the Wildlife Trade Regulations, requires an NDF by importing Member States and therefore monitors newly established quotas and changes to previous quota levels to assess the situation where necessary, or to reassess SRG opinions or EU decisions. Similarly, by assessing the new quotas early each year, the SRG can advise on the treatment of anticipated import applications within the EU.

Export quotas are usually established by each Party to CITES unilaterally on a voluntary basis, but they can also be set by the Conference of the Parties, or result from recommendations of the and Committees. To ensure that national quotas are effectively communicated and implemented on permits and certificates, countries should inform the CITES Secretariat when they establish national export quotas for CITES species (Resolution Conf. 12.3 (Rev. CoP16)). In turn, the Secretariat informs the Parties by publishing a list of national export quotas of which it has been informed ( www..org/eng/resources/quotas/index.php ).

Quotas generally relate to a calendar year (1 st of January to 31 st of December); however, since 2008 sturgeon quotas have related to a ‘quota year’ (1 st March to last day of February). For species of Acipenseriformes, quotas should be established and communicated to the CITES Secretariat for meat and caviar from stocks shared between different Range States (Resolution Conf. 12.7 (Rev. CoP16)). Guidance on the ‘ Management of nationally established export quotas’ is available through Resolution Conf. 14.7 (Rev. CoP15).

In 2014, quotas were published on the CITES website ( www.cites.org ) on 14/03/2014 and were updated on 26/03/2014, 14/04/2014 and 20/06/2014.

Based on the quotas that were available on 28/04/2014, UNEP-WCMC analysed the 2014 CITES export quotas to identify:

a) Quotas that were newly established in 2014 (i.e. 2014 quotas for particular species/country/term/source combinations which have not previously been subject to a quota, or have not been subject to a quota for at least the last 5 years);

b) Quotas that increased or decreased in 2014 compared with 2013 quotas (or compared with 2012 quotas if no quota was published in 2013).

This analysis was discussed at SRG 68 on 28/05/2014 and a list of 18 taxa/country combinations that may warrant review was presented; in addition Member States were invited to suggest any additional species with new or increased quotas that may warrant review. The following species are reviewed in this report: Brookesia overview

• Brookesia betschi/ (new quota, 300 live) • Brookesia ebenaui/Madagascar (new quota, 150 live) 5 • Brookesia grivaudi/Madagascar (new quota, 150 live) • Brookesia minima/ Madagascar (new quota, 150 live) • Brookesia nasus/Madagascar (new quota, 150 live) • Brookesia peyrierasi/ Madagascar (new quota, 150 live) • Brookesia therezieni/Madagascar (increased quota, 500 live) • Calumma parsonii/Madagascar (increased quota, 300 live) • Ravenea rivularis/Madagascar (increased quota, 4500 kg seeds)

The SRG agreed that further consideration might be necessary to determine whether the trade would have a harmful effect on the conservation status of these species or on the extent of the territory occupied by the relevant population of these species. These reviews are presented below. Additional species/country combinations are planned for review for SRG 70. Update since Analysis of 2014 CITES export quotas

Since the publication of the Analysis of 2014 CITES export quotas (UNEP-WCMC, 2014) additional CITES export quotas were published from Botswana, Cameroon, the Democratic Republic of Congo, Georgia, Honduras, Indonesia, Jamaica, Mozambique, Paraguay and Romania on 20 th June 2014. Of these, the following relate to new or increased quotas of note:

An increase in quotas for various wild-taken species from Indonesia, namely: 11 250 skins and skin products of Python breitensteini (increased from 10 800 skins and skin products in 2013); 2700 skins and skin products of Python curtus (increased from 1890 skins and skin products in 2013); and 28 500 live, wild-taken pieces (not identifiable to species level) of Fungia spp. (increased from 24 500 live, wild-taken pieces in 2013). In addition, there was an increase in the quota for Panthera leo from Mozambique, from 50 wild-taken specimens in 2012 and 2013 to 53 wild-taken specimens in 2014.

The following new quotas were published: 12 915 live Cyclemys dentata from Indonesia (LR/nt); 4500 live Dogania subplana from Indonesia (LR/lc); 4000 pieces of live, wild-taken Acanthophyllia deshayesiana (NT – as Cynarina lacrymalis ) from Indonesia; 616 wild-taken Papio cynocephalus (LC) from Mozambique; 41 wild-taken Philantomba monticola (LC) from Mozambique; 1 400 000 kg of wood and 250 000 kg of extract of Bulnesia sarmientoi from Paraguay (LR/cd) (positive opinion formed 28/05/2014).

In addition, CITES export quotas relating to sturgeon and paddlefish were published on the CITES website on 10 th June 2014. The only increased or new quotas related to aquacultured specimens from Iran.

Of the taxa for which new or increased quotas have been published in 2014 at the species level, Cyclemys dentata and Dogania subplana may warrant further consideration by the SRG, as these species were listed in the CITES Appendices at CoP16 and their Red List assessments are outdated. Acanthophyllia deshayesiana from Indonesia may also warrant review, given the relatively high new quota and potential taxonomic confusion with Cynarina lacrymalis , for which an EU suspension is in place. References UNEP-WCMC. 2014. Analysis of 2014 CITES export quotas . UNEP-WCMC, Cambridge Brookesia overview

Brookesia spp.: Overview of status, management 6 and trade.

The Malagasy leaf (Brookesia spp.) are dwarf chameleons endemic to Madagascar; they are generally small (ca. 30-110 mm total length), cryptic and ground-dwelling, living in leaf litter by day and climbing into low vegetation at night (Tolley and Burger, 2007; Glaw and Vences, 2007). The CITES standard nomenclatural references recognise 26 Brookesia species (Glaw et al. , 1999; Klaver and Böhme, 1997), with 30 species currently recognised by Uetz and Hallerman (2014). Many of the species occur in northern Madagascar, where they are restricted to small regions of rainforest and occupy relatively narrow elevational ranges, resulting in a high degree of regional endemicity (Raxworthy and Nussbaum, 1995).

Whilst there are many studies focusing on site-specific inventories of Brookesia , there is far less information available about the abundance, density or population trends of individual species (Carpenter and Robson, 2005; Jenkins et al. , 1999), or on how chameleons respond to habitat disturbance (Jenkins et al., 2003).

Brookesia species are considered to be forest specialists, hence they are vulnerable to forest fragmentation and degradation (Randrianantoandro et al. , 2008; Raselimanana and Rakotomalala, 2003). Collection for trade was also considered a threat (Carpenter and Robson, 2005), with chameleons being perhaps the most targeted of Madagascar’s herpetofauna (Jenkins et al. , 1999; Raselimanana and Rakotomalala, 2003; Glaw and Vences, 2007 in: Lowin, 2012).

Madagascar ratified CITES in 1975. Following a period of political instability in 2002, the CITES Management Authority introduced a six-month moratorium on all international trade in native species of fauna and flora (Rabesihanaka et al. , 2008). In accordance with the recommendations of the CITES Animals and Plants Committees, a Review of Significant Trade was conducted at the country level in Madagascar, which resulted in the creation of a CITES Action Plan for the reform of Madagascar’s wildlife export and the establishment of an operational Scientific Authority (Rabesihanaka et al. , 2008). Concurrently, Madagascar adopted several pieces of legislation relating to wildlife trade (Ministère de l’Environnement des Eaux et Forets, 2006):

• Act No. 2005-018 of 17 October 2005 on International Trade and of Wild Fauna and Flora; • Decree No. 2006-097 of 31 January 2006 laying down detailed rules for implementing the Act No. 2005-018 of 17 October 2005; • Decree No. 2006-098 of 31 January 2006 concerning the publication of the revised Appendices to CITES; • Decree No. 2006-400 from 13 June 2006 on the classification of species of wildlife. The wildlife species of Madagascar are classified into three categories: protected (Category 1), harmful (Category 2) and game (Category 3). Under Decree No. 2006-400, Brookesia perarmata is classified as a Category 1, Class 1 (protected) species, which strictly prohibits the hunting, capture, detention and commercial trade of the species; 24 Brookesia species are classified as Category 1, Class 2 (protected) species (including B. betschi, B. ebenaui, B. griveaudi, B. minima, B. nasus and B. therezieni , all reviewed in this current report 1), which means authorisation from the relevant in-country CITES authorities is required for the collection of the species from the wild (Ministère de l’Environnement des Eaux et Forets, 2006).

1 Brookesia peyrierasi, also reviewed in this report, is not listed in Decree No. 2006-400. Brookesia overview

The CITES Scientific Authority of Madagascar (Dr Falitiana Rabemananjara in. litt. to UNEP- WCMC, 17 July 2014) confirmed that the 2014 export quotas for species were set 7 cautiously, based on their IUCN Red List categorisation, as follows:

and Endangered species – zero quota

• Vulnerable species – 150 live specimens

• Near Threatened – 150 to 300 live specimens

• Least Concern – 500 live specimens

Madagascar published fifteen zero export quotas for Brookesia species in 2014.

Dr Richard Jenkins and Dr Frank Glaw (Jenkins pers. comm. to UNEP-WCMC, 31 July 2014) considered that the quotas set for the seven Brookesia species reviewed in this report were likely to be sustainable. However, they expressed concern whether, for some of the species ( B. betschi, B. ebenaui, B. minima ), collectors would be able to find sufficient collection localities outside of protected areas. Dr F. Glaw (Jenkins pers. comm. to UNEP-WCMC, 31 July 2014) also noted a potential lookalike issue in distinguishing some of the species from their closest relatives, although considering the size of the quotas, this was not thought to pose a serious problem for species conservation. Dr R. Jenkins (pers. comm. to UNEP-WCMC, 31 July 2014) also raised the potential concern that if there was demand for certain species that could not be legally collected [such as the Brookesia species with zero quotas], there might be trade in threatened species under different trade names if traded species cannot be easily identified.

Trade at the level

The genus Brookesia was listed in CITES Appendix II in 2003 (except for B. perarmata, which was listed in Appendix I). Over the period 2003-2012 there was a small amount of trade at the genus level from Madagascar to the EU-28 (wild-sourced bodies to Germany and Italy), and to the rest of the world (wild-sourced bodies, live individuals and scientific specimens, all to the United States), all of which was for scientific purposes (Table 1). No indirect exports of Brookesia spp. to the EU-28 originating in Madagascar were reported 2003-2012.

Table 1: Direct exports of Brookesia spp . from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced for scientific purposes. (No trade was reported in 2011).

Importer Term Unit Reported by 2003 2004 2005 2006 2007 2008 2009 2010 2012 Total

EU bodies - Importer 11 5 3 26 11 56 Exporter 5 26 14 8 71 124 RoW bodies - Importer Exporter 23 11 80 114 live - Importer Exporter 23 23 specimens ml Importer Exporter 37 37 - Importer 1 11 27 39 Exporter 1 1 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014. Brookesia overview

REPTILIA: CHAMAELEONIDAE 8 Brookesia betschi II/B

COMMON NAMES: Blanc's leaf chameleon (English)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Near Threatened

Taxonomic Note Glaw and Vences (2007) noted that the of Brookesia betschi was in need of revision. Trade patterns Madagascar published a new CITES export quota of 300 live specimens of Brookesia betschi in 2014. The only reported direct export of B. betschi from Madagascar to the EU-28 over the period 2003-2012 comprised two wild-sourced bodies for scientific purposes in 2005, reported by both Madagascar and Germany. Direct trade to the rest of the world 2003-2012 comprised two wild- sourced scientific specimens imported by the United States in 2004 (reported as 2 mg of scientific specimens by Madagascar) and six wild-sourced scientific specimens imported by the United States in 2008 (not reported by Madagascar). No indirect exports of B. betschi to the EU-28 originating in Madagascar were reported 2003-2012. Conservation status Brookesia betschi is restricted to northern Madagascar (Andreone, 2004; Raxworthy and Nussbaum, 1995; Klaver and Böhme, 1997), where it occurs in montane humid forest between 1150 and 1650 m altitude (Jenkins et al ., 2011).

It was reported to occur in (Raxworthy and Nussbaum, 1995; Klaver and Böhme, 1997; Glaw and Vences, 2007; Andreone et al. , 2000), Tsaratanana (Raxworthy and Nussbaum, 1995; Klaver and Böhme, 1997; Glaw and Vences, 2007), Manongarivo Special Reserve (Glaw and Vences, 2007), and Anjanaharibe-Sud Special Reserve (Glaw and Vences, 2007; Andreone et al. , 2000). It was also found in other forests between these protected areas (Andreone et al. , 2000; Glaw and Vences, 2007). All records to date were reported to be from primary or mature secondary forest (Jenkins et al ., 2011). Brookesia betschi

B. betschi is categorised as Near Threatened in the IUCN Red List, and the species’ range area and the quality of its habitat are continuing to decline (Jenkins et al., 2011). Its extent of occurrence 9 was estimated to be 11 090 km 2, although this includes degraded land between forest blocks (Jenkins et al ., 2011). It was considered to have a decreasing population trend due to the loss of rainforest habitat in northern Madagascar (Jenkins et al ., 2011).

The main threats to forests where B. betschi occurs were reported to include slash and burn agriculture and timber extraction (Jenkins et al ., 2011).

Jenkins et al . (2011) reported that the species was protected in Madagascar, but could be collected with authorization from outside of protected areas. It was noted that research was needed into population trends and the species’ distribution between known sites (Jenkins et al ., 2011).

Brookesia ebenaui

REPTILIA: CHAMAELEONIDAE 10 Brookesia ebenaui II/B

COMMON NAMES: Northern leaf chameleon (English), Brookésie d'Ebenau (French)

SYNONYMS: Brookesia legendrei , Chamaeleo ebenaui

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Vulnerable

Trade patterns Madagascar published a new CITES export quota of 150 live specimens of Brookesia ebenaui in 2014. Direct exports of B. ebenaui from Madagascar to the EU-28 over the period 2003-2012 comprised small numbers of wild-sourced bodies to Germany and Italy and live individuals to Germany (reported by Madagascar only) (Table 1). Direct trade from Madagascar to the rest of the world 2003-2012 comprised small numbers of wild-sourced live individuals and scientific specimens to the United States. No indirect exports of B. ebenaui to the EU-28 originating in Madagascar were reported 2003-2012.

Table 1: Direct exports of Brookesia ebenaui from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced. (No trade was reported 2005-2006 or 2008-2012).

Importer Term Purpose Reported by 2003 2004 2007 Total

EU bodies S Importer 2 1 3 Exporter 3 1 4 live T Importer Exporter 25 25 RoW live T Importer Exporter 25 25 specimens S Importer 2 2 Exporter 2 2 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014.

Conservation status Brookesia ebenaui is restricted to the far north of Madagascar, in low- or mid-altitude dry and humid forests (Glaw and Vences, 2007; Jenkins et al. , 2011f), occurring at a maximum elevation of 950 m above sea level (Raxworthy and Nussbaum, 1995). It was described as the most arboreal Brookesia species, also being arboreal during the day (Glaw and Vences, 2007).

It was reported to occur in Montagne d’Ambre National Park (Raxworthy and Nussbaum, 1994, 1995; Glaw and Vences, 2007; Durkin et al. , 2011), Lokobe Strict Nature Reserve, Nosy Be (Andreone et al. , 2003; Glaw and Vences, 2007; Raxworthy and Nussbaum, 1995), Montagne des Français (D’Cruze et al. , 2008; Glaw and Vences, 2007), Fontenay Nature Park (D’Cruze et al. , 2008), Manongarivo Special Reserve (Jenkins et al. , 2011f) and Ankarana Special Reserve (Raxworthy and Nussbaum, 1995). Brookesia ebenaui

The species was reported to be locally common, but with a decreasing population trend (Jenkins et al. , 2011f). B. ebenaui was recorded as ‘rare’ during 2005-2006 surveys of the Montagne des 11 Français massif in the Antsiranana region, where it was found at an altitude of 140 m in forest habitat (D’Cruze et al. , 2007). In the Forêt d’Ambre Special Reserve, at the foot of the Montagne d’Ambre mountain complex in the Antsiranana region it was recorded as ‘common’ (D’Cruze et al. , 2008).

B. ebenaui is categorised as Vulnerable in the IUCN Red List, as it has a severely fragmented population and there is continued decline in the extent and quality of its habitat within its estimated range area (14 321 km 2), due to agricultural activities and logging (Jenkins et al. , 2011f).

The main threats to the species were reported to include forest loss and degradation due to, among other factors, agricultural clearance, charcoal and timber production, cattle grazing (D’Cruze et al. , 2007, 2008; Jenkins et al. , 2011f), small-scale quarrying, and small-holder development (Jenkins et al. , 2011f).

Jenkins et al. (2011e) noted that more information was needed on this species' distribution and population status, and on the extent and intensity of various threats within its range. Brookesia griveaudi

REPTILIA: CHAMAELEONIDAE 12 Brookesia griveaudi II/B

COMMON NAMES: Marojejy leaf chameleon (English)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Near Threatened

Trade patterns Madagascar published a new CITES export quota of 150 live specimens of Brookesia griveaudi in 2014. Direct exports of B. griveaudi from Madagascar to the EU-28 over the period 2003-2012 comprised small numbers of wild-sourced bodies to Germany and Italy, and scientific specimens to Portugal (Table 1). Direct trade from Madagascar to the rest of the world 2003-2012 comprised wild-sourced scientific specimens to the United States. No indirect exports of B. griveaudi to the EU-28 originating in Madagascar were reported 2003-2012.

Table 1: Direct exports of Brookesia griveaudi from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced for scientific purposes. (No trade was reported 2006-2007, 2009-2010 or 2012).

Importer Term Unit Reported by 2003 2004 2005 2008 2011 Total

EU bodies - Importer 2 2 Exporter 2 2 4 specimens - Importer 6 6 Exporter RoW specimens mg Importer Exporter 13 13 - Importer 14 7 21 Exporter 1 1 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014.

Conservation status Brookesia griveaudi was reported to be common in low-altitude rainforest of northeast Madagascar (Glaw and Vences, 2007; Raxworthy and Nussbaum, 1995), up to a maximum elevation of 1350 m above sea level (Jenkins et al. , 2011b).

It was reported to occur in Marojejy National Park (Andreone et al. , 2000; Glaw and Vences, 2007; Raxworthy and Nussbaum, 1995), Tsararano Forest (Andreone et al. , 2000; Glaw and Vences, 2007), Masoala National Park (Glaw and Vences, 2007; Raxworthy and Nussbaum, 1995), as well as Antalaha, Fanano, Maroantsetra and Sambava forests (Glaw and Vences, 2007).

B. griveaudi is categorised as Near Threatened in the IUCN Red List, with a severely fragmented population and continuing decline in the area and quality of its forest habitat, due to logging and slash-and-burn agriculture (Jenkins et al. , 2011b). Its extent of occurrence was estimated to be 21 829 km 2. The species was reported to have a decreasing population trend (Jenkins et al. , 2011b). Brookesia griveaudi

Jenkins et al. (2011a) noted that whilst the species occurs in several protected areas, management of these sites and protection of additional remnant forest may be required. 13 Brookesia griveaudi

REPTILIA: CHAMAELEONIDAE 14 Brookesia minima II/B

COMMON NAMES: Minute leaf chameleon (English), Brookésie naine (French)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Vulnerable

Taxonomic Note Within the Brookesia genus are a number of highly miniaturised species, known as the Brookesia minima group (Brygoo and Domergue, 1975), which was originally composed of five very small species with a snout-vent length of 14–30 mm (Brookesia dentata, B. minima, B. peyrierasi, B. ramanantsoai and B. tuberculata ) (Brygoo, 1978 in: Glaw et al. , 2012). Species within this group have proved difficult to distinguish, due to low morphological differences and retainment of paedomorphic [juvenile] features, with many of the characters used to identify larger Brookesia species being greatly reduced within the B. minima group (Glaw et al. , 1999).

The original CITES standard nomenclatural reference for Brookesia spp. (Klaver and Böhme, 1997) considered Brookesia peyrierasi and B. tuberculata to be synonyms of B. minima . However, B. peyrierasi and B. tuberculata have since been elevated to distinct species and have a separate CITES standard nomenclatural reference (Glaw et al. , 1999, adopted at CoP16).

Jenkins et al. (2011f) advised that “The taxonomy of the B. minima group is in need of revision and the distribution of all species needs to be re-evaluated following thorough morphometric and molecular studies.” Trade patterns Madagascar published a new CITES export quota of 150 live specimens of Brookesia minima in 2014. Direct exports of B. minima from Madagascar to the EU-28 over the period 2003-2012 comprised small numbers of wild-sourced bodies to Germany and live individuals to Germany and the United Kingdom (Table 1). Direct trade from Madagascar to the rest of the world 2003- 2012 comprised wild-sourced live individuals to the United States and Japan and scientific specimens to the United States. No indirect exports of B. minima to the EU-28 originating in Madagascar were reported 2003-2012. Brookesia minima

Table 1: Direct exports of Brookesia minima from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced. (No trade was reported 15 2007-2009 or 2011-2012).

Importer Term Purpose Reported by 2003 2004 2005 2006 2010 Total

EU bodies S Importer 5 1 6 Exporter 4 5 9 live T Importer 6 25 31 Exporter 25 75 100 RoW live T Importer 30 50 80 Exporter 85 85 specimens S Importer 2 2 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014.

Conservation status Brookesia minima is restricted to the northwest of Madagascar (Andreone, 2004; Glaw and Vences, 2007; Glaw et al. , 1999), inhabiting leaf litter of low-altitude rainforest of the Sambirano region (Glaw and Vences, 2007). Individuals have been recorded from sea level to 750 m altitude (Jenkins et al. , 2011g).

Due to difficulties in species identification, and the recognition of B. peyrierasi and B . tuberculara as distinct species, there are few confirmed localities for B. minima (Jenkins et al. , 2011g). It was reported to occur on the island of Nosy Be, including Lokobe Strict Nature Reserve (Glaw and Vences, 2007; Andreone et al. , 2003), Manarikoba forest (Glaw and Vences, 2007) and Manongarivo Special Reserve (Glaw and Vences, 2007; Glaw et al. , 1999). It was recently also found at Sahamalaza-îles Radama National Park (Raselimanana, 2008 in: Jenkins et al. , 2011f), whilst its presence in Tsaratanana Reserve was reported to require confirmation (Jenkins et al. , 2011g).

B. minima is categorised as Vulnerable in the IUCN Red List, as it has a severely fragmented population and there is continued decline in the extent and quality of its habitat within its estimated range (14 321 km 2), due to slash-and burn agricultural and logging (Jenkins et al. , 2011g). The species, described as “not common”, was reported to have a decreasing population trend (Jenkins et al. , 2011g).

Threats to the species were reported to include slash and burn agriculture and logging for charcoal production and construction materials (Jenkins et al. , 2011g).

Jenkins et al. (2011e) noted that research was needed to clarify the taxonomy and distribution of B. minima , as well as this species' exposure to and sensitivity to threats.

Brookesia nasus

REPTILIA: CHAMAELEONIDAE 16 Brookesia nasus II/B

COMMON NAMES: Elongate leaf chameleon (English)

SYNONYMS: Brookesia betsileana

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Vulnerable

Taxonomic Note Whilst the current CITES standard nomenclatural reference, Klaver and Böhme (1997), includes Brookesia nasus in the genus Brookesia , recent research into chameleon phylogeny has identified B. nasus and B. lolontany as a sister clade, clearly seperated from all other Brookesia species (Townsend et al. , 2009; Tolley et al. , 2013). Glaw et al. (2013) subsequently transfered B. nasus and B. lolontany to the genus , producing two clearly monophyletic genera (Vences et al. , 2013). Trade patterns Madagascar published a new CITES export quota of 150 live specimens of Brookesia nasus in 2014. Direct exports of B. nasus from Madagascar to the EU-28 over the period 2003-2012 comprised small numbers of wild-sourced bodies to Germany and Italy (Table 1). Direct trade from Madagascar to the rest of the world 2003-2012 comprised wild-sourced bodies and scientific specimens to the United States. No indirect exports of B. nasus to the EU-28 originating in Madagascar were reported 2003-2012.

Table 1: Direct exports of Brookesia nasus from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced for scientific purposes. (No trade was reported in 2008 0r 2010-2012).

Importer Term Unit Reported by 2003 2004 2005 2006 2007 2009 Total

EU bodies - Importer 1 2 3 Exporter 3 2 2 7 RoW bodies - Importer Exporter 3 3 specimens mg Importer Exporter 4 87 91 - Importer 22 80 4 106 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014.

Conservation status Brookesia nasus occurs in of southeastern Madagascar (Klaver and Böhme, 1997; Glaw and Vences, 2007). It was reported to inhabit humid forests spanning elevations of 410-1920 m in low, mid and high altitude vegetation types (Nussbaum et al. , 1999; Raxworthy and Nussbaum, 1996 in: Jenkins et al. , 2011c). Brookesia nasus

It was reported to occur in a number of localities including Kalambatritra Special Reserve (Andreone and Randrianirina, 2007), Andohahela, Andringitra and Ranomafana National Parks 17 (Andreone and Randrianirina, 2007; Glaw and Vences, 2007), forest fragments in Mandena and Sainte Luce (Lehtinen et al. , 2003; Lehtinen and Ramanamanjato, 2006) and from Ambahaka forest, Ambalamarovandana, Andrambovato, Eminiminy, Ikongo, Ivohibe camp, Manambolo, Tolagnaro, Vinanitelo and Vohiparara (Glaw and Vences, 2007).

B. nasus was reported to occur at a relatively high abundance in Andohahela (Andreone and Randriamahazo, 1997 in: Jenkins et al. , 2011c). It was found to be the most abundant chameleon during surveys of Ranomafana National Park, 1993-1994, with population densities of 26.8 ha -1 (95% C.I. 17.7-40.5 ha -1) recorded (Jenkins et al. , 1999). Mandena was reported to represent the southern limit of the species’ distribution (Ramanamanjato, 2007); B. nasus was reported to be localised in the largest blocks of closed-canopy littoral forest, whilst being absent from smaller forest patches (Ramanamanjato, 2007). The species was reported to have a decreasing population trend (Jenkins et al. , 2011d).

A subspecies, B. nasus pauliani, was described from montane forest of the Andringitra mountains, but it was not found during recent surveys and its taxonomic status requires clarification (Glaw and Vences, 2007; Raxworthy and Nussbaum, 1996; Jenkins et al. , 2011d).

B. nasus (as Palleon nasus ) is categorised as Vulnerable in the IUCN Red List, as there is continued decline in the extent and quality of its habitat within its estimated range area (15 798 km 2), due to slash-and burn agriculture, logging for charcoal and mining, and it is thought to occur as a severely fragmented population (Jenkins et al. , 2011d).

Jenkins et al. (2011c) noted that whilst the species occurs in several protected areas, management of these sites and protection of additional sites may be required. Research was recommended to investigate its life history and to monitor population trends (Jenkins et al. , 2011d). Brookesia peyrierasi

REPTILIA: CHAMAELEONIDAE 18 Brookesia peyrierasi II/B

COMMON NAMES: Antongil leaf chameleon (English)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Endangered 2

Taxonomic Note Brookesia peyrierasi was formerly considered a synonym of B. minima (e.g. Raxworthy and Nussbaum, 1995), but was resurrected following examination of additional collection specimens and identification of differences in both external and genital morphology (Schimmenti and Jesu, 1996; Glaw et al. , 1999 [CITES standard nomenclatural reference for the species]). Trade patterns Madagascar published a new CITES export quota of 150 live specimens of Brookesia peyrierasi in 2014. There was no reported direct or indirect trade of B. peyrierasi from Madagascar to the EU-28 or the rest of the world, over the period 2003-2012. However, the CITES standard nomenclatural reference recognising B. peyrierasi as distinct from B. minima was only adopted at CoP16 in 2013. Conservation status Brookesia peyrierasi occurs in the northeast of Madagascar (Andreone, 2004; Glaw and Vences, 2007; Glaw et al. , 1999). It was reported to occur on Nosy Mangebe (Glaw and Vences, 2007; Glaw et al. , 1999; Raxworthy, 1988), in Anandrivola forest (Glaw and Vences, 2007; Raxworthy, 1988) and Masoala National Park (Glaw and Vences, 2007). A confirmed 2010 record was reported from a locality west of Maroansetra, close to Makira Reserve (F. Glaw pers. comm., January 2011, in: Jenkins et al. , 2011g). Jenkins et al. (2011g) also listed several other localities, which require verification due to taxonomic uncertainties within the B. minima group.

B. peyrierasi was reported to have been recorded at high densities on Nosy Mangabe (Lutzman, 2006 in: Jenkins et al. , 2011g), and to be common in the rainforest leaf litter of Nosy Mangabe (Glaw and Vences, 2007). The species was reported to have a decreasing population trend (Jenkins et al ., 2011h).

B. peyrierasi is provisionally categorised as Endangered in the IUCN Red List, as its population is severely fragmented and there is continued decline in the extent and quality of its habitat within its estimated range area (3774 km 2), due to mining and selective logging for rosewood (Jenkins et al. , 2011h). It was noted that the species may occur more widely than its current tentative estimated range area (although probably not more widely than 20 000 km²), pending resolution of outstanding taxonomic issues (Jenkins et al. , 2011h).

2 The IUCN Red List status for Brookesia peyrierasi originally displayed incorrectly as Vulnerable on the website, in contrast to the status of Endangered given in the justification. This was confirmed to be an error (Jenkins, R. pers. comm. to UNEP-WCMC, 26 June 2014), which was corrected in version 2014.2 of the Red List, available from 24 July 2014. Brookesia peyrierasi

Threats to the species were reported to include loss, degradation and fragmentation of lowland forest, resulting from rosewood extraction and mining for precious stones (Jenkins et al. , 2011h). 19

The CITES SA of Madagascar (Dr Falitiana Rabemananjara pers. comm. to UNEP-WCMC, 17 July 2014) confirmed that quotas for chameleons were set cautiously, based on their Red List status – for which Endangered and Critically Endangered species have been assigned a zero quota (see Brookesia overview section). However, whilst B. peyrierasi is categorised provisionally as Endangered, its status was displaying incorrectly as Vulnerable on the IUCN Red List website 2; the quota of 150 live specimens was therefore set based on this assumption. 3

B. peyrierasi is not listed among the Brookesia species protected under Madagascar’s national legislation (Decree No. 2006-400)(Ministère de l’Environnement des Eaux et Forets, 2006), presumably because it was formerly considered a synoym of B. minima . The CITES SA of Madagascar (Dr Falitiana Rabemananjara pers. comm. to UNEP-WCMC, 17 July 2014) confirmed that the species was “under consideration” in terms of the national legislation.

Jenkins et al. (2011g) noted that further research was needed into this species' distribution, population status, ecology and sensitivity to forest degradation, as well as clarification of the taxonomy of members of the B. minima group.

3 The Scientific Authority of Madagascar have since been informed of this issue. Brookesia therezieni

REPTILIA: CHAMAELEONIDAE 20 Brookesia therezieni II/B

COMMON NAMES: Perinet leaf chameleon (English)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: -

IUCN: Least Concern

Trade patterns Madagascar published a CITES export quota of 500 live specimens of Brookesia therezieni in 2014; quotas of 100 live specimens were published each year from 2005 to 2013 (Table 1). According to data reported by Madagascar, the 2010 export quota appears to have been exceeded by 14 individuals; however, Madagascar has indicated that some annual reports (including the 2010 report) have been based on permits issued, rather than actual trade.

Table 1: CITES export quotas for live, wild-sourced Brookesia therezieni from Madagascar and global direct exports of live individuals, as reported by the countries of import and export, 2005-2014. (Trade data for 2013 and 2014 are not yet available.)

2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

Quota 100 100 100 100 100 100 100 100 100 500 Reported by the importers 2 31 66 37 62 53 86 93 Reported by Madagascar 39 88 79 100 72 114 79 88

Direct exports of B. therezieni from Madagascar to the EU-28 over the period 2003-2012 mainly comprised wild-sourced live individuals to Germany, Czech Republic, the Netherlands, France, Spain and Italy (Table 2). Direct trade from Madagascar to the rest of the world 2003-2012 mainly comprised wild-sourced live individuals to the United States, Japan and Canada. No indirect exports of B. therezieni to the EU-28 originating in Madagascar were reported 2003-2012.

Table 2: Direct exports of Brookesia therezieni from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012.

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

EU bodies S W Importer 1 4 5 Exporter 2 1 3 live T W Importer 10 32 37 36 33 57 51 256 Exporter 25 19 39 51 43 40 51 52 38 358 RoW bodies T I Importer 1 1 Exporter live T I Importer 4 4 Exporter W Importer 2 21 34 26 20 29 42 174 Exporter 20 49 28 57 32 63 27 50 326 specimens S W Importer 10 1 11 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014. Brookesia therezieni

Conservation status 21 Brookesia therezieni occurs in mid-altitude rainforest of eastern Madagascar (Klaver and Böhme, 1997; Glaw and Vences, 2007) at altitudes between 900 and 1500 m above sea level (Jenkins et al. , 2011c).

It was reported to occur in Anjanaharibe-Sud Special Reserve (Andreone et al. , 2000), Mantadia National Park, Andasibe Analamazaotra Special Reserve (Jenkins et al. , 2011c; Glaw and Vences, 2007) and in the areas of An'Ala, Ankeniheny and Imerimandroso in eastern Madagascar (Glaw and Vences, 2007). Rabearivony and Thorstrom (2010) also reported its occurrence in Bemanevika (a protected area in process of creation) in northwestern Madagascar. The species was reported to be relatively abundant in the southern part of its range (Jenkins et al. , 2011c).

B. therezieni is categorised as Least Concern in the IUCN Red List, as although its habitat is declining and the population is likely to be fragmented, it has a relatively large distribution (extent of occurrence >30 000 km 2) (Jenkins et al. , 2011c). The species was reported to have a decreasing population trend (Jenkins et al. , 2011c).

Threats to the species were reported to include rainforest loss through land clearance and slash- and-burn farming (Jenkins et al. , 2011c).

Jenkins et al. (2011b) noted that further research should be carried out into the harvest levels and population trends of the species. B. therezieni was reported to be difficult to distinguish in the field from sympatrically living B. superciliaris (Ratsoavina et al., 2010), although this species is also categorised as Least Concern (Jenkins et al. , 2011a). Brookesia references

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Lowin, A. J. 2012. Chameleon species composition and density estimates of three unprotected dry deciduous forests between Montagne d ’ Ambre Parc National and Ankarana Réserve 24 Spéciale in northern Madagascar. Herpetology Notes , 5, p.107–113. Lutzman, N. 2006. Untersuchungen zur Ökologie der Chamäleonfauna der Masoala-Halbinsel, Nord-Ost Madagaskar . Mathematisch-Naturwissenschaftlichen Fakultät, Rheinischen Friedrich-Wilhelms-Universität Bonn. Ministère de l’Environnement des Eaux et Forets. 2006. Manuel de procédures pour la gestion de la faune et de la flore sauvages de Madagascar . USAID. p.111. Nussbaum, R. A., Raxworthy, C. J., Raselimanana, A. P. and Ramanamanjato, J. B. 1999. Amphibians and reptiles of the Réserve Naturelle Intégrale d’Andohahela, Madagascar. In A floral and faunal inventory of the Réserve Naturelle Intégrale d'Andohahela, Madagascar: with reference to elevational variation. Fieldiana Zoology , 94, p.155–173. Rabearivony, J. and Thorstrom, R. 2010. Protected area surface extension in Madagascar: Do and threatened species remain useful criteria for site selection? Madagascar Conservation & Development , 5 (1), p.35–47. Rabemananjara, F. 2014. Dr Falitiana Rabemananjara (CITES Scientific Authority of Madagascar) in. litt. to UNEP-WCMC, 17 July 2014. Rabesihanaka, S. S., Rakouth, B., Ravavaripalala, A., Rarivoson, T. I., Rabouth, H., Ravaomanalina, H., Rabotondrazaby, A. and Rabesoa, R. 2008. Evaluation de la politique nationale du commerce des especes sauvages - Madagascar . UNEP-UNCTAD CBTF, CITES & IUED. Available at: http://www.cites.org/common/prog/policy/madagascar.pdf (English version). Rakotoarivelo, A. R., Razafimanahaka, J. H., Rabesihanaka, S., Jones, J. P. G. and Jenkins, R. K. B. 2011. Lois et règlements sur la faune sauvage à Madagascar: Progrès accomplis et besoins du futur. Madagascar Conservation & Development , 6 (1), p.37–44. Ramanamanjato, J. 2007. and amphibian communities along the humidity gradient and fragmentation effects in the littoral forests of southeastern Madagascar. In: Ganzhorn, J. U., Goodman, S. M. and Vincelette, M. (eds.), Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin) , Smithsonian Institution, p.167–180. Randrianantoandro, J. C., Randrianavelona, R., Andriantsimanarilafy, R. R., Hantalalaina, E. F., Rakotondravony, D., Randrianasolo, M., Ravelomanantsoa, H. L. and Jenkins, R. K. B. 2008. Identifying important areas for the conservation of dwarf chameleons ( Brookesia spp.) in Tsingy de Bemaraha National Park, western Madagascar. Oryx , 42 (4), p.578–583. Raselimanana, A. P. 2008. Herpétofaune des forêts sèches malgaches. Malagasy Nature , 1, p.46–75. Raselimanana, A. P. and Rakotomalala, D. 2003. Chamaeleonidae, chameleons. In: Goodman, S. M. and Benstead, J. P. (eds.), The natural history of Madagascar , Chicago, USA: The University of Chicago Press, p.961–969. Ratsoavina, F. M., Ranaivoarisoa, F. J., Rafeliarisoa, T. H., Crottini, A., Louis Jr, E. E. and Vences, M. 2010. Molecular phylogeography of a widespread Malagasy leaf chameleon species, Brookesia superciliaris. Zootaxa , 2554, p.62–64. Raxworthy, C. J. 1988. Reptiles, rainforest and conservation in Madagascar. Biological conservation , 43, p.181–211. Raxworthy, C. J. and Nussbaum, R. A. 1995. systematics, speciation and biogeography of the dwarf chameleons (Brookesia , Reptilia, Squamata, Chamaeleontidae) of northern madagascar. Journal of Zoology , 235, p.525–558. Raxworthy, C. J. and Nussbaum, R. A. 1996. Amphibians and reptiles of the Réserve Naturelle Intégrale d’Andringitra, Madagascar: a study of elevational distribution and local endemnicity. Fieldiana Zoology , 85, p.158–170. Raxworthy, C. and Nussbaum, R. A. 1994. A rainforest survey of amphibians, reptiles and small mammals at Montagne d’Ambre, Madagascar. Biological Conservation , 69 (1994), p.65–73. Brookesia references

Schimmenti, G. and Jesu, R. 1996. Brookesia exarmata sp. nov. (Reptilia, Chamaeleonidae): a new dwarf chameleon from the limestone outcrops of western Madagascar. Italian Journal of 25 Zoology , 63 (2), p.193–197. Tolley, K. A., Townsend, T. M. and Vences, M. 2013. Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proceedings of the Royal Society Biological Sciences , 280 no. 1759 p. 1-8.. Tolley, K. and Burger, M. 2007. Chameleons of Southern Africa . Cape Town, South Africa: Struik Publishers. Townsend, T. M., Vieites, D. R., Glaw, F. and Vences, M. 2009. Testing species-level diversification hypotheses in Madagascar: the case of microendemic Brookesia leaf chameleons. Systematic biology , 58 (6), p.641–656. Uetz, P. and Hallermann, J. 2014. The . Available at: www.reptile-database.org [Accessed: 26 June 2014]. Vences, M., Guayasamin, J. M., Miralles, A. and de la Riva, I. 2013. To name or not to name: criteria to promote economy of change in Linnaean classification schemes. Zootaxa , 3636 (2), p.201–244.

Calumma parsonii

REPTILIA: CHAMAELEONIDAE 26 Calumma parsonii II/B

COMMON NAMES: Parson’s giant chameleon (English), Caméléon de Parson (French), Camaleón de Parson (Spanish)

SYNONYMS: Chamaeleo madecasseus, Chamaeleo parsonii

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: Current no opinion (i) for Madagascar formed on 07/02/2013 (comes into effect upon removal from the Suspensions Regulations).

4.6(b) import suspension for wild specimens from Madagascar first applied on 19/09/1999 and last confirmed on 10/09/2012.

IUCN: Near Threatened

Taxonomic Note There are two recognised subspecies, Calumma parsonii parsonii and Calumma parsonii cristifer (Klaver and Böhme, 1997), the latter occurs around Analamazaotra and Mantadia (Jenkins et al. , 2011). At least three distinct colour morphs are known (Brady and Griffiths, 1999; Glaw and Vences, 2007). Trade patterns A CITES trade suspension for several Calumma species (including C. parsonii ) formed in 1995 under the Review of Significant Trade process was withdrawn in 2012, following endorsement of zero export quotas established for several Calumma species, including C. parsonii (Notification No. 2012/048, AC26 Summary Record). In 2014, Madagascar published a CITES export quota of 300 C. parsonii , following zero quotas published for the species in 2012 and 2013.

There were virtually no direct exports of C. parsonii from Madagascar to the EU-28 over the period 2003-2012, other than a few wild-sourced bodies to Italy and Germany for scientific purposes and the seizure of one live individual reported by Austria (Table 1). Likewise, there was very little direct trade from Madagascar to the rest of the world 2003-2012, other than a small number of wild-sourced bodies and specimens traded for scientific purposes, all to the United States. No indirect exports of C. parsonii to the EU-28 originating in Madagascar were reported 2003-2012.

Calumma parsonii

Table 1: Direct exports of Calumma parsonii from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. (No trade was reported in 2005, 2007, 2009 or 2011- 27 2012).

Importer Term Unit Purpose Source Reported by 2003 2004 2006 2008 2010 Total

EU bodies - S W Importer 1 1 Exporter 2 2 live - - I Importer 1 1 Exporter RoW bodies - S W Importer 1 1 Exporter 9 9 specimens mg S W Importer Exporter 0.9 0.9 - S W Importer 10 3 3 1 17 Exporter Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 17/06/2014.

Conservation status Calumma parsonii is one of the world’s largest chameleons, exceeding 60 cm in total length (Tolley and Burger, 2007; Glaw and Vences, 2007). It is considered to be particularly long-lived, reaching an age of 10-12 years (Glaw and Vences, 2007).

Little information was available on the life history or reproduction of C. parsonii. However, under captive conditions, females were reported to produce a single clutch per year, with each clutch containing 30-60 eggs (Brady and Griffiths, 1999). In captivity, eggs were reporteded to be buried 30 cm into the ground, with incubation requiring the alternation of warm and cold periods; juveniles were reported to hatch after 400-520 days (Glaw and Vences, 2007). Anecdotal evidence indicated that sexual maturity does not usually occur until 3-5 years after hatching (A. Abate, pers. comm. in: Brady and Griffiths, 1999). The species was reported to survive well in captivity but to breed poorly (Brady and Griffiths, 1999).

The species inhabits mid- and low-altitude rainforest and forest edges, especially along forest streams, and is widespread across northern and eastern Madagascar (Glaw and Vences, 2007). It was reported to occur at elevations from 45 to 1195 m (Jenkins et al. , 2011). Jenkins et al. ( 2011) reported C. parsonii to range from “Ranomafana in the south to Anjanaharibe Sud in the north (Rakotomalala and Raselimanana, 2003) and the Masoala Peninsula (F. Andreone pers. comm. January 2011). It has also been recorded from Manongarivo in the northwest (Raxworthy et al. , 2003).” Glaw and Vences (2007) reported the species’ occurrence in: Ambolokopatrika, Ambanja, Ambavaniasy, Ambodifotatra, Analamazoatra, Andasibe, Anjanaharibe-Sud, Antsihanaka, Fanovana, Fenoarivo, Ifanadiana, Ikongo, Kianjavato, Mananjary, Nosy Boraha, near Ifanadiana, Sahatavy Ouest, Sahembendrana, Tsaramandroso and Vavatenina.

The species was reported to occur in a number of strictly protected areas (Jenkins et al. , 2011), with C. parsonii cristifer occurring in Mantadia National Park and Analamazaotra Special Reserve (Rakotondravony, 2004; Rakotomalala and Raselimanana, 2003 in: Rabearivony et al. , 2007).

Glaw and Vences (2007) reported that C. parsonii cristifer was regularly seen on larger branches of bushes and at 2-4 m height at night. In the Ranomafana region, eastern Madagascar, C. parsonii was reported to be “very rare in dense primary rainforest, but ... regularly found in disturbed rainforest and rainforest edges at lower elevations” (Glaw and Vences, 2007). C. parsonii parsonii was described as a rare member of the community in relatively intact forest of the Ambodiriana Private Reserve within Ambodiriana forest, eastern Madagascar (Rabearivony et al. , 2007). Few C. parsonii parsonii were reported to have been found during qualitative surveys of nine locations within its recorded range conducted 1996-1997, with most observations coming Calumma parsonii

from small fragments of forest in Ifanadiana and Nosy Boraha (Abate, 1998 in: Brady and Griffiths, 1999). C. parsonii cristifer was reported to occur at densities of between 1.3 and 3.9 individuals per 28 ha in relatively intact forest of the Mantadia region, eastern Madagascar, with lower densities in more disturbed regions (0.4-1.1 per ha), based on surveys conducted 1998-99 (Brady and Griffiths, 1999). These population densities were notably lower than for some other Calumma species within the region (Brady and Griffiths, 1999). Brady and Griffiths (1999) estimated the national population size of C. parsonii to be between a minimum of 3.8 and maximum of 37.4 million individuals (based on multiplying minimum and maximum densities from estimates taken from five different sites, by the total area of remaining suitable habitat within the species known range - 38 624 km 2). The species was reported to have a decreasing population trend (Jenkins et al. , 2011).

C. parsonii is categorised as Near Threatened in the IUCN Red List, based on a past population decline of greater than 15-20 per cent, due mainly to habitat loss driven by slash-and-burn agriculture and other threats across its large range (Jenkins et al. , 2011).

Main threats to the species were reported to include the loss of humid forest due to slash-and- burn agriculture and logging, particularly given that this large chameleon occurring at low densities is unlikely to persist in small forest fragments (Jenkins et al. , 2011). Collection for the international pet trade was also noted as a potential threat, if not managed properly; large-scale collection of wild individuals prior to the 1995 trade suspension was noted to have likely been a contributor to localised declines (Jenkins et al. , 2011).

The species was reported to have been collected in large numbers in the 1990s, from locations including Ifanadiana, Tolongoina, Ranomafana (outside the National Park), Ambatoharanana- Ambositra, Soanieran’Ivongo, Maroantsetra and Antalaha (Ravoninjatovo and Rabemananjara, 1999 in: Brady and Griffiths, 1999). Brady and Griffiths (1999) considered the trade levels [several thousand individuals per year] prior to the moratorium on trade in Chamaeleo spp. (CITES notification No. 833 20/01/1995) to be of concern, given the low densities of the species in the Mantadia region, high prices commanded by the species outside Madagascar and reports of decreasing abundance of C. p. parsonii in areas most heavily collected (Ravoninjatovo and Rabemananjara, 1999 in: Brady and Griffiths, 1999). They cautioned that “Given the relatively long time that C. p. parsonii requires to reach adulthood, any form of commercial exploitation that involves the collection of sexually mature individuals (especially females) could have an adverse effect on wild populations” (Brady and Griffiths, 1999).

Illegal collection for the pet trade may also pose a threat; a TRAFFIC survey of the trade in Malagasy reptiles and amphibians in Thailand conducted in January 2010 found 28 C. parsonii among the 115 Calumma individuals encountered (Todd, 2011). Specimens were estimated to fetch retail prices of 621 USD in northern Europe and 485 USD in Thailand (Todd, 2011).

Under Decree No. 2006-400, C. parsonii is classified as a Category 1, Class 2 (protected) species, which means authorisation from the relevant in-country CITES authorities is required for collection of the species from the wild (Ministère de l’Environnement des Eaux et Forets, 2006).

The Standing Committee’s withdrawal of the CITES trade suspension for C. parsonii (and other Calumma species) in 2012 was based on a number of conditions, including: establishment of a conservative export quota; conducting a status assessment and developing a population monitoring programme for the species; and basing any changes to the annual export quota on the results of this assessment and monitoring programme (SC62 Doc. 27.2). In 2014, the CITES Scientific Authority of Madagascar informed UNEP-WCMC that their 2014 annual export quota of 300 C. parsonii was set cautiously, based on its IUCN Red List categorisation of Near Threatened (Dr Falitiana Rabemananjara, pers. comm. to UNEP-WCMC, 17 July 2014). Calumma parsonii

Dr Richard Jenkins and Dr Frank Glaw (Jenkins pers. comm. to UNEP-WCMC, 31 July 2014) expressed some concern regarding the size of the 2014 export quota, given that C. parsonii is long- 29 lived and occurs at low densities, hence being at greater risk from over-collection than species with shorter life cycles. Dr R. Jenkins (pers. comm. to UNEP-WCMC, 31 July 2014) also noted that C. parsonii was close to qualifying for Vulnerable status (Jenkins et al ., 2011), and suggested that a lower quota may be more prudent. He suggested that it would be useful to have information on proposed collection sites (given that C. parsonii occurs in many protected areas) and on whether adults or juveniles would be targeted for collection, as well as whether mortality and potential illegal trade had been considered during quota-setting (Dr R. Jenkins, pers. comm. to UNEP- WCMC, 31 July 2014). References Abate, A. 1998. Reports from the field; Parson’s chameleon. Chameleon Information Network , 29, p.17–25. Brady, L. D. and Griffiths, R. A. 1999. Status assessment of chameleons in Madagascar . IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, UK. Glaw, F. and Vences, M. 2007. A field guide to the amphibians and reptiles of Madagascar . 3rd ed. Cologne: Vences & Glaw Verlag, p.495. Jenkins, R. 2014. Richard Jenkins (Chair, IUCN Chameleon Specialist Group), pers. comm. to UNEP-WCMC, 31/07/2014. Jenkins, R. K. B., Andreone, F. Andriamazava, A. Anjeriniaina, M., Brady, L., Glaw, F., Griffiths, R. A., Rabibisoa, N., Rakotomalala, D. Randrianantoandro, J. C. and Randrianiriana, J. Randrianizahana , H. Ratsoavina, F. Robsomanitrandrasana, E. 2011. Calumma parsonii. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.1 . Available at: www.iucnredlist.org [Accessed: 25 June 2014]. Klaver, C. J. J. and Böhme, W. 1997. Chamaeleonidae. In: Wermuth, H. (ed.), Das Tierreich, Part 112 , Berlin and New York: Verlag Walter de Gruyter & Co. Ministère de l’Environnement des Eaux et Forets. 2006. Manuel de procédures pour la gestion de la faune et de la flore sauvages de Madagascar . USAID. p.111. Rabearivony, J., Brady, L. D., Jenkins, R. K. B. and Ravoahangimalala, O. R. 2007. Habitat use and abundance of a low-altitude chameleon assemblage in eastern Madagascar. Herpetological Journal , 17, p.247–254. Rakotomalala, D. and Raselimanana, A. P. 2003. Les amphibiens et reptiles des massifs de Marojejy, d’Anjanaharibe-Sud et du couloir forestier de Betaolana. In: Goodman, S. M. and Wilme, L. (eds.), Nouveaux résultats d’inventaires biologiques faisant référence à l’altitude dans la région des massifs montagneux de Marojejy et d’Anjanaharibe-Sud , Antananarivo, p.146–202. Rakotondravony, H. 2004. Diversité des caméléons forestiers de la région d’Andasibe (Madagascar) et modèle de distribution de cette communauté selon différent types physionomiques. La Terre et la Vie: Revue d’Ecologie , 59, p.529–544. Ravoninjatovo, A. and Rabemananjara, F. 1999. Evaluation of chameleon network in Madagascar . Unpublished Report, Université de Antananarivo, Madagascar. Raxworthy, C. J., Martinez-Meyer, E., Horning, N., Nussbaum, R. a, Schneider, G. E., Ortega- Huerta, M. a and Townsend Peterson, a. 2003. Predicting distributions of known and unknown reptile species in Madagascar. Nature , 426 (6968), p.837–841. Todd, M. 2011. Trade in Malagasy Reptiles and Amphibians in Thailand . Petaling Jaya, Selangor, Malaysia: TRAFFIC Southeast Asia, Petaling Jaya, Selangor, Malaysia, p.30. Tolley, K. and Burger, M. 2007. Chameleons of Southern Africa . Cape Town, South Africa: Struik Publishers.

Calumma parsonii

ARECALES: PALMAE 30 Ravenea rivularis II/B

COMMON NAMES: Majesty palm (English)

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: Current positive opinion for wild specimens from Madagascar formed on 29/02/2008

IUCN: Endangered

Trade patterns Ravenea rivularis was listed in CITES Appendix II in 2003. Madagascar published a CITES export quota of 4500 kg of seeds of R. rivularis in 2014; the only previous quota for the species was a zero quota published in 2013. Direct exports of R. rivularis from Madagascar to the EU-28 over the period 2003-2012 mainly comprised wild-sourced seeds to the Netherlands for commercial purposes, reported in 2007 and 2010 only (Table 1). Direct trade from Madagascar to the rest of the world 2003-2012 consisted entirely of wild-sourced seeds exported for commercial purposes, mainly to the United States. Indirect exports of R. rivularis to the EU-28 originating in Madagascar 2003-2012 consisted of live, wild-sourced individuals (Table 2), all re-exported by the United States to the Netherlands for commercial purposes.

Table 1: Direct exports of Ravenea rivularis from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was wild-sourced.

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

EU live - G Importer 3 3 Exporter seeds kg T Importer 1000 1000 Exporter 4000 1000 5000 RoW seeds kg T Importer 1500 4058 3475 4570 4925 3575 4350 4825 6550 2000 39828 Exporter 1500 3475 1350 4925 3675 4350 4825 7250 2000 33350 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 25/06/2014.

Table 2: Indirect exports of Ravenea rivularis from Madagascar to the EU-28, 2003-2012. All trade was wild-sourced for commercial purposes. (No trade was reported 2003-2006 or 2011).

Term Reported by 2007 2008 2009 2010 2012 Total live Importer 200 1000 250 1450 Exporter 2300 2550 8100 5050 250 18250 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 25/06/2014.

Ravenea rivularis

Conservation status Ravenea rivularis is a palm growing up to 30m in height, which has become a popular ornamental (Jones, 1994). Females produce bright red fruits, each containing a single seed, which are collected for export (Beentje, 1994a). The seeds were reported not to preserve particularly well and to have relatively low germination rates after drying (Rakotondranony et al. , 2006).

R. rivularis is endemic to southwestern Madagascar, between the Isalo, Sakaraha and Analavelona mountains (Rakotoarinivo and Dransfield, 2012). It grows on river banks in slow-moving, shallow water in areas of lowland forest between 300 and 1000 m and it can occur in dense stands (Beentje, 1994a; Rakotoarinivo and Dransfield, 2012). Beentje (1994b) described the species as “not common in the wild, but where it grows it can often be found in large stands, along rivers or swamp margins.” It was previously thought to be limited to two populations totalling about 60 trees (Dransfield and Beentje, 1995 in: CITES CoP12 Prop. 60), but Rakotoarinivo and Dransfield (2012) estimated the total population to be about 900 trees. The most recent information from CITES Scientific Authority of Madagascar (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014), extracted from a report produced for CITES in 2013, confirmed there to be a total of 17 known sub-populations, including nine studied subpopulations; two sub-populations were reported to occur in protected areas. The 2014 quota for R. rivularis was set based on an estimate of 16 794 mature individuals (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014). The species was reported to occur at an estimated density of 2450 individuals/ha at an oasis around Sakaraha and Zombitse-Vohibasia National Park in southern Madagascar, with a regeneration rate of 64 per cent (which was considered low) (SC65 Inf. 2).

R. rivularis is categorised as Endangered in the IUCN Red List, with the justification that its populations were known from only a limited area of occurrence (2122 km²) and occupancy (144 km²) in southwestern Madagascar, with continuing decline in the extent and quality of its habitat and of mature individuals, and a decreasing population trend (Rakotoarinivo and Dransfield, 2012). The CITES Scientific Authority of Madagascar (Aro Vonjy in. litt . to UNEP- WCMC, 21 July 2014) reported slightly different figures, with an extent of occurrence of 5486 km² and area of occupancy of 60 km².

The main threats to remaining populations of R. rivularis were reported to be loss of habitat due to agriculture, logging, and mining for sapphires (Rakotoarinivo and Dransfield, 2012). Harvesting of seeds may also impact the regeneration of existing stands (Rakotoarinivo and Dransfield, 2012).

Sapphire mining sites around R. rivularis were reported to hinder regeneration, due to gravel being left at the foot of trees (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014). The CITES SA of Madagascar have recommended planting of R. rivularis around sapphire mines, to address some of the damage caused to young individuals (SC65 Inf. 2).

It is one of the most sought after palm species from Madagascar in international horticulture, and although there are trade regulations in place, illegal harvest of seed from the wild was still reported to occur (Rakotoarinivo and Dransfield, 2012).

R. rivularis was selected for the CITES Review of Significant Trade following CoP14 (PC18 Doc 8.4), following which the species was reviewed by UNEP-WCMC (PC19 Doc 12.3 Annex 3) and categorised as ‘Possible Concern’ (PC19 Summary Record). Madagascar was required to: inform the Secretariat of methodology used for making non-detriment findings; review available information and establish a conservative export quota; and prepare a draft management plan for trade in wild seeds of palms, for review at the 20 th meeting of the Plants Committee (PC19 Summary Record). Madagascar established a zero quota for the species in December 2012, pending results of studies comissioned by the Secretariat (SC63 Doc. 14). In February 2014, the Management Authority of Madagascar submitted a report on implementation of Ravenea rivularis

recommendations by the Plants Committee, including a proposed quota of 4500 kg of seeds, following which it was determined that the recommendations had been implemented and the 32 Secretariat notified Madagascar in March 2014 that the species had been removed from the review process (SC65 Inf. 2; SC65 Doc. 26.1). Harvest quotas were reported to be set based on the number of mature individuals, seed weight per plant per year and the level of threat, with 20 per cent of seeds left on the plants for regeneration 4; the export quota is then 90 per cent of the harvest quota, to allow for seeds that fail to germinate 5 (SC65 Inf. 2; Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014).

R. rivularis is not included under Decree No. 2006-400 (Ministère de l’Environnement des Eaux et Forets, 2006), hence is not legally protected in Madagascar. However, export of seeds requires a permit issued by the forestry authority and any export must be validated by the Scientific Authority (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014).

4 The harvest quota was set based on the formula Qp= (S x P x Me x 80%)/3 , where S is the estimated number of mature individuals, P is the seed weight per plant per year and Me is the threat level (low: 0.25; medium: 0.5; high: 0.75). Hence Qp= (16 794 x 2.25 x 0.5 x 80%)/3 = 5038 kg (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014).

5 The export quota was set based on the formula Qe = Qp x 90% . Hence Qe = 5038 x 90% = 4534, giving an annual export quota of 4500 kg of seeds (Aro Vonjy in. litt . to UNEP-WCMC, 21 July 2014). Ravenea rivularis

References Beentje, H. J. 1994a. A monograph of Ravenea (Palmae: ). Kew Bulletin , 49 (4), p.623–671. Beentje, H. J. 1994b. Ravenea in Madagascar. Principes , 38 (4), p. 193-203. Dransfield, J. and Beentje, H. 1995. The Palms of Madagascar . Royal Botanic Gardens, Kew and The International Palm Society. Jones, D. 1994. Palms throughout the world. Chatswood, NSW, p.410. Ministère de l’Environnement des Eaux et Forets. 2006. Manuel de procédures pour la gestion de la faune et de la flore sauvages de Madagascar . USAID. p.111. Rakotoarinivo, M. & Dransfield, J. 2012. Ravenea rivularis . In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.1. < www.iucnredlist.org >. Downloaded on 24 June 2014. Rakotondranony, G.L., Sacande, M., Wood, C. and Pritchard, H. 2006. Seed storage responses in four species of the threatened genus Ravenea (). Seed Science and Technology , 34, p.513–517. Vonjy, A. 2014. Aro Vonjy (Madagascar Scientific Authority) in. litt . to UNEP-WCMC, 21 July 2014.

Appendix

34 Appendix 34 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