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Home , Oophaga, Oophaga sylvatica, Phyllobates aurotaenia

Review of selected on the basis of a new or increased export quota in 2013

(Version edited for public release)

Prepared for the

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

by the

United Nations Environment Programme World Conservation Monitoring Centre

November, 2013

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The United Nations Environment Programme PREPARED FOR World Conservation Monitoring Centre (UNEP- WCMC) is the specialist assessment The European Commission, Brussels, Belgium centre of the United Nations Environment Programme (UNEP), the world’s foremost DISCLAIMER intergovernmental environmental organisation. The contents of this report do not necessarily reflect The Centre has been in operation for over 30 years, the views or policies of UNEP, contributory combining scientific research with practical policy organisations or editors. The designations advice. The Centre's mission is to evaluate and employed and the presentations do not imply the highlight the many values of biodiversity and put expressions of any opinion whatsoever on the part authoritative biodiversity knowledge at the centre of UNEP, the European Commission or of decision-making. Through the analysis and contributory organisations, editors or publishers synthesis of global biodiversity knowledge the concerning the legal status of any country, territory, Centre provides authoritative, strategic and timely city area or its authorities, or concerning the information for conventions, countries and delimitation of its frontiers or boundaries. The organisations to use in the development and mention of a commercial entity or product in this implementation of their policies and decisions. publication does not imply endorsement by UNEP. UNEP-WCMC provides objective and scientifically rigorous procedures and services. These include © Copyright: 2013, European Commission ecosystem assessments, support for the implementation of environmental agreements, global and regional biodiversity information, research on threats and impacts, and the development of future scenarios.

CITATION

UNEP-WCMC. 2013. Review of species selected on the basis of a new or increased export quota in 2013. UNEP-WCMC, Cambridge.

Table of Contents

Introduction ...... 4

Update since Analysis of 2013 CITES export quotas ...... 4

SPECIES: Agalychnis spurrelli ...... 5

SPECIES: sylvatica ...... 8

Annex I: Key to purpose and source codes ...... 11

Introduction

Introduction 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 Plants Committees. Guidance on the management of nationally established export quotas is available through Resolution Conf. 14.7 (Rev. CoP15). To ensure that national quotas are effectively communicated, 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. Early each year, the Secretariat publishes a Notification to the Parties containing a list of export quotas of which it has been informed. Quotas generally relate to a calendar year (1st January to 31st December); however, since 2008 sturgeon quotas have related to a quota year (1st March to last day of February). In 2013, quotas were published on the CITES website (www..org) on 11/04/2013 and were updated on 28/06/2013, 02/07/2013, 12/07/2013, 30/08/2013 and 17/09/2013. Based on the quotas that were available on 09/05/2013, UNEP-WCMC analysed the 2013 CITES export quotas to identify: a) Quotas that were newly established in 2013 (i.e. 2013 quotas for particular species/country/term/source combinations which had not previously been subject to a quota, or had not been subject to a quota for at least the last 5 years); b) Quotas that increased or decreased in 2013 compared with 2012 quotas (or compared with 2011 quotas if no quota was published in 2012). This analysis was discussed at SRG 64 on 28/05/2013. At that meeting, one species/country combination was selected for review (Pseudoscaphirhynchus kaufmanni from Uzbekistan) where a the new quota in 2013 indicated that further consideration might be necessary to determine whether trade would have a harmful effect on the of the species or on the extent of the territory occupied by the relevant population of the species. This review was provided in an SRG 65 document. Update since Analysis of 2013 CITES export quotas Since publication of the Review of species selected on the basis of new or increased CITES export quotas in 2013: Pseudoscaphirhynchus kaufmanni from Uzbekistan & Update to the 2013 quota analysis (SRG65), which contained an update on new and increased export quotas published until 06/08/2013, additional CITES export quotas have been published on the CITES website (as of 20/09/2013). Of these, the following relate to new or increased quotas: an increase in live Hippocampus comes from Viet Nam from 11 000 in 2012 to 13 000 in 2013; new zero export quotas for Diospyros spp. and Dalbergia spp. from Madagascar and new quotas for 450 live captive-bred auratus, 620 live captive-bred aurotaenia and 240 live captive-bred Phyllobates terribilis from . The published quota for Crocodylus niloticus from Mozambique decreased from 1800 wild-taken specimens in 2012 to 1500 wild-taken specimens in 2013. At SRG 65, two further taxa were selected for review due to newly published quotas. These were:  Agalychnis spurrelli / Ecuador: New quota of 3000 live individuals. Categorized as Least Concern by the IUCN.  / Ecuador: New quota of 400 live individuals. Categorized as Near Threatened by the IUCN.

Trade data included in this report were downloaded from the CITES Trade Database on 23/09/2013.

Agalychnis spurrelli

REVIEW OF SPECIES SELECTED ON THE BASIS OF A NEW OR INCREASED EXPORT QUOTA IN 2013

AMPHIBIA HYLIDAE

SPECIES: Agalychnis spurrelli

SYNONYMS: Agalychnis litodryas, Phyllomedusa spurrelli, Phyllomedusalito dryas

COMMON NAMES: Gliding Leaf (English), Grenouille d’arbre de spurelli (French), Rana deslizadora (Spanish)

RANGE STATES: Colombia, Costa Rica, Ecuador, Panama

RANGE STATE UNDER REVIEW: Ecuador

IUCN RED LIST: Least Concern

TRADE PATTERNS: Ecuador: Agalychnis spurrelli was listed in CITES Appendix II on 23/06/2010 and in Annex B of the EU Wildlife Trade Regulations on 10/08/2010. Ecuador published a CITES export quota for 3000 live, wild- sourced specimens in 2013; no quotas were published in previous years. According to data in the CITES Trade Database, no direct or indirect trade in the species nor in the genus originating in Ecuador has been reported; Ecuador’s annual reports for 2006, 2011 and 2012 have not yet been received, and trade data for 2013 are not yet available. TAXONOMIC NOTE The standard CITES nomenclature reference for Amphibia recognises Agalychnis litodryas, Phyllomedusa spurrelli and Phyllomedusa litodryas as synonyms of A. spurrelli (Frost, 2013). Ortega- Andrade (2008) also placed A. litodryas as a junior synonym of A. spurrelli. However, the IUCN recognised A. litodryas as a separate species (Coloma et al., 2004), although in the IUCN Red List classification for A. spurrelli it was noted that more than one species may currently be included within A. spurrelli (F. Bolaños pers. comm. in Jungfer et al., 2004). CONSERVATION STATUS in range states A. spurrelli is a medium-large sized arboreal frog species, found in the humid lowlands and lower premontane zone forests (altitudinal range of 15-750 m) of central western Costa Rica, through Panama and Colombia to northwestern Ecuador (Duellman, 1970; Frost, 2013; Jungfer et al., 2004; Savage, 2002; Vega et al., 2009). The species was reported to breed explosively during the rainy season, when large numbers congregate around ponds (Gomez-Mestre and Warkentin, 2007; Jungfer et al., 2004; Vargas et al., 2000). Mean clutch size was reported as 76.8 (Gomez-Mestre and Warkentin, 2007). The main threats to the species were considered to be for agricultural development, illegal crops, logging, human settlement and pollution resulting from the spraying of illegal crops (Jungfer et al., 2004). Chytridiomycosis was found in museum specimens of A. spurrelli, but the impact of this fungal disease on wild populations was unknown (Jungfer et al., 2004). A. spurrelli was classified as Least Concern by the IUCN, based on the fact that it had a wide distribution, the population was presumed to be large and because it was considered unlikely to be declining fast enough to qualify for a more threatened category (Jungfer et al., 2004). The species’

Agalychnis spurrelli

abundance was reported to be unclear and its arboreal habits mean it is rarely seen, but the overall population trend was considered to be one of decline (Jungfer et al., 2004). The IUCN recognised and assessed A. litodryas as a separate species and classified it as Vulnerable (Coloma et al., 2004). A. spurrelli is similar in appearance to other Agalychnis spp. and was included in the proposal document for addition onto Appendix II on the basis that it was a look-alike species, although it was also noted that obvious markings on each species enabled identification for enforcement purposes (CoP15 Prop.13). It was noted that A. spurrelli was occasionally traded but that information on the species was scarce (CoP15 Prop.13). Ecuador: The range of A. spurrelli in Ecuador was reported to cover an area of 19 600 km2 in the northwestern part of the country; it has been recorded from at least 22 locations, along the Pacific coast and inland (Ortega-Andrade, 2008). Field surveys in Esmeraldas Province recorded the species at the Bilsa Biological Station (Ortega-Andrade et al., 2010) and in San Francisco del Cabo (particularly in La Laguna del Diablo), where the population size was estimated to be 1400-6000 individuals (Ortega- Andrade et al., 2011). Ortega-Andrade (2008) noted that the species may have been “locally abundant”, even in disturbed areas, and while it was difficult to observe during field studies, it was considered unlikely that there were undiscovered populations in northwestern Ecuador. The species was categorised nationally as Least Concern by Ron and Read (2011) and more recently as Near Threatened by Coloma et al. (2013). The tropical forest of A. spurrelli in Ecuador was considered to be declining dramatically and becoming increasingly fragmented as a result of deforestation (Ortega-Andrade et al., 2011; Ortega-Andrade, 2008; Ron and Read, 2011; Zambrano- Barragán, 2010). The illegal trade of wild-caught to the US and European pet markets from Ecuador was also considered to be of concern by the Ministry of Environment of Ecuador (Ministerio del Ambiente, 2012). Two populations of A. spurrelli were found to occur in the vicinity of the Reserva Ecologica Cotacachi- Cayapas, although the areas in question were subject to selective logging, vegetation removal for agriculture and pressure from agricultural expansion and human settlements (Ortega-Andrade, 2008). The species was also found in some private reserves, e.g. Bilsa Biological Station (Ortega-Andrade, 2008). Outside of reserves, areas where the species was found were reported to often be subject to severe environmental degradation and habitat loss (Ortega-Andrade, 2008). Ortega-Andrade et al. (2011) noted that there were no specific strategies relating to the conservation of the species in Ecuador, but that it was potentially a good candidate for management as it could adapt well to a variety of non-forest environments, as long as water was present nearby. The commercial export of wild-sourced specimens of wild fauna and flora is reportedly only authorised if the specimens are managed as part of approved in situ management programmes (Ministerio del Ambiente, 2011; Republic of Ecuador, 2003). Wikiri was reported to be the only company allowed to export amphibians from Ecuador (Ministerio del Ambiente, 2012). REFERENCES: Coloma, L. A., Guayasamin, J. M., and Menéndez-Guerrero, P. (2013). Lista Roja de Anfibios de Ecuador. Quito, Ecuador: AnfibiosWebEcuador, Fundación Otonga. URL: http://anfibioswebecuador.ec/listaroja/listaroja_spp.aspx?Id=176 Accessed: 23/10/2013. Coloma, L. A., Ron, S., Jungfer, K., Cisneros-Heredia, D., Almendáriz, A., Solís, F., Ibáñez, R., Jaramillo, C. and Fuenmayor, Q. (2004). Agalychnis litodryas. In: IUCN Red List of Threatened Species. Version 2013.1. IUCN Red List of Threatened Species. Version 2013.1. URL: www.redlist.org Accessed: 20/09/2013. Duellman, W. E. (1970). The Hylid of Middle America. Monograph of the Museum of Natural History, The University of Kansas, 1, 1–753. Frost, D. R. (2013). Species of the World: an Online Reference. Version 5.6 (9 January 2013). New York, USA: American Museum of Natural History. URL: http://research.amnh.org/herpetology/amphibia/index.html Accessed: 20/09/2013.

Agalychnis spurrelli

Gomez-Mestre, I., and Warkentin, K. M. (2007). To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs. Oecologia, 153, 197–206. Jungfer, K., Bolívar, W., Kubicki, B., Bolaños, F., Chaves, G., Solís, F., Ibáñez, R., Savage, J., Jaramillo, C. and Fuenmayor, Q. (2004). Agalychnis spurrelli. In: IUCN Red List of Threatened Species. Version 2013.1. URL: www.redlist.org Accessed: 20/09/2013. Ministerio del Ambiente. (2008). Situación actual del tráfico ilegal de la vida silvestre (p. 52). Dirección Nacional de Biodiversidad Unidad de Vida Silvestre. Ministerio del Ambiente. (2011). Manual para exportación de flora y fauna silvestre en el Ecuador (p. 26). Dirección Nacional de Biodiversidad Unidad de Vida Silvestre. Ministerio del Ambiente. (2012). Oficio Nro. MAE-DNB-2012-0408: Exportación ilegal de anfibios. Dirección Nacional de Biodiversidad. Ortega-Andrade, H. M. (2008). Agalychnis spurrelli Boulenger (Anura, Hylidae): variacion, distribucion y sinonimia. Papeis Avulsos de Zoologia, 48(13), 103–117. Ortega-Andrade, H. M., Bermingham, J., Aulestia, C., and Paucar, C. (2010). Herpetofauna of the Bilsa Biological Station, province of Esmeraldas, Ecuador. Check List, 6(1), 119–154. Ortega-Andrade, H. M., Tobar-Suarez, C., and Arellano M. M. (2011). Tamano poblacional, uso del habitat y relaciones interspecificas de Agalychnis spurrelli (Anura: Hylidae) en un bosque humedo tropical remanente del noroccidente de Ecuador. Papeis Avulsos de Zoologia, 51(1), 1–19. Republic of Ecuador. (2003). Decreto No 3.516 - Biodiversidad (Libro IV, Títulos I a VII, del Texto Unificado de la Legislación Secundaria del Ministerio del Ambiente). Ron, S. R., and Read, M. (2011). Agalychnis spurrelli. In S. R. Ron, J. M. Guayasamin, M. H. Yanez-Munoz, and A. Merino-Viteri (Eds.), AmphibiaWebEcuador. Museo de Zoologia, Pontificia Universidad Catolica de Ecuador. URL: http://zoologia.puce.edu.ec/vertebrados/anfibios/FichaEspecie.aspx?Id=1278. Accessed: 01/10/2013. Savage, J. M. (2002). The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas (p. 934). University of Chicago Press. Vargas, S. F., Bolanos, M. E., and Berrio-B, H. (2000). Notas sobre la ecologia reproductiva de Agalychnis spurrelli (Anura: Hylidae) en una poblacion de Anchicaya, Pacifico Colombiano. Revista de la Academia Colombiana de Ciencias Exactas Fisicas y Naturales, 24(90), 85–99. Vega, A., Robertson, J. M., and Chaves, G. (2009). Agalychnis spurrelli. Herpetological Review, 40(3), 361. Zambrano-Barragán, C. (2010). National Forest and Climate Policy in Ecuador: Perspectives for REDD+ and Social Participation (p. 42). Programa Derechos, Cambio Climático y Bosques ECUADOR.

Oophaga sylvatica

REVIEW OF SPECIES SELECTED ON THE BASIS OF A NEW OR INCREASED EXPORT QUOTA IN 2013

AMPHIBIA HYLIDAE

SPECIES: Oophaga sylvatica

SYNONYMS: Dendrobates histrionicus, Dendrobates histrionicus sylvaticus

RANGE STATES: Colombia, Ecuador

RANGE STATE UNDER REVIEW: Ecuador

IUCN RED LIST: Near Threatened

TRADE PATTERNS: Ecuador: Oophaga sylvatica was listed in CITES Appendix II on 22/10/1987 and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997. Ecuador published a CITES export quota for 400 live, wild-sourced specimens in 2013; no quotas were published in previous years. According to data in the CITES Trade Database, no direct trade in the species or at genus level from Ecuador was reported 2003-2012. Ecuador’s annual reports for 2006, 2011 and 2012 have not yet been received, and trade data for 2013 are not yet available. The only indirect trade in the species reported over the period 2003-2012 consisted of 13 live, captive-bred specimens re-exported via Canada to Japan for commercial purposes in 2011, reported by the importer only (reported as Dendrobates histrionicus). TAXONOMIC NOTE Following CoP16, there was a genus split of Oophaga spp. from Dendrobates spp., and O. sylvatica was transferred from Dendrobates and split from D. histrionicus (AC26 Doc 20); D. histrionicus is now considered a synonym of O. histrionica (CoP16 Doc. 43.1 (Rev. 1). Coloma et al., (2004) highlighted the possibility that O. sylvatica is a complex of several species, with “true” O. sylvatica occurring only in Ecuador. CONSERVATION STATUS in range states O. sylvatica is a diurnal frog species, found in the lowland and submontane rainforests of southwestern Colombia and northwestern Ecuador, up to altitudes of 1000 m (Coloma et al., 2004; Ortiz et al., 2013). Ortiz et al. (2013) noted that the species could also survive well in moderately disturbed areas. While the species was considered common in Colombia, numbers were reported to have declined in Ecuador and the overall population trend was one of decline (Coloma et al., 2004; Ortiz et al., 2013). The main threats to O. sylvatica were reported to be deforestation for agricultural development, cultivation of illegal crops, logging, mining, human settlements and pollution resulting from spraying of illegal crops (Ortiz et al., 2013). O. sylvatica was classified as Near Threatened by the IUCN and it was noted that although the species had a relatively wide distribution, the serious declines in Ecuador meant that its overall status was of concern (Coloma et al., 2004). Ecuador: O. sylvatica was reported from northwestern Ecuador, in the provinces of Pichincha, Esmeraldas, Imbabura, Santo Domingo de los Tsáchilas, Cotopaxi, and Los Ríos (Ortiz et al., 2013).

Oophaga sylvatica

Hamilton et al. (2005) recorded D. sylvaticus in field surveys in 2004 at Hacienda Siberia, a humid forest site in Manibi Province, and noted that the study area was subject to disturbance by cattle, deforestation and development. Ortega-Andrade et al. (2010) recorded O. sylvatica in surveys at Bilsa Biological Station, Esmeraldas Province, within forest and stream . No information on population estimates could be found for this species in Ecuador. Nationally, the species was classified as Least Concern by Ortiz et al., 2013 but as Near Threatened by Coloma et al. (2013). Numbers of O. sylvatica were reported to have seriously declined (Coloma et al., 2004). The illegal trade of wild-caught amphibians to the US and European pet markets from Ecuador was also considered to be of concern by the Ministry of Environment of Ecuador (Ministerio del Ambiente, 2012). The commercial export of wild-sourced specimens of wild fauna and flora is reportedly only authorised if the specimens are managed as part of approved in situ management programmes (Ministerio del Ambiente, 2011; Republic of Ecuador, 2003). Wikiri was reported to be the only company allowed to export amphibians from Ecuador (Ministerio del Ambiente, 2012). The range of the species was reported to overlap with the Reserva Ecológica Cotacachi-Cayapas and the Parque Nacional Mache-Chindul (Coloma et al., 2004). Coloma et al. (2004) noted that management practices which could allow a sustainable commercial harvest of the species should be investigated. In the proposal document to include Dendrobates spp. in Appendix II of CITES, it was noted that these species were relatively easy to breed and keep in captivity, although captive populations had a tendency to collapse after a few generations, requiring further wild specimens to be collected (CoP6 Prop.47). However, it has also been reported that the specialised diet of D. histrionicus tadpoles, consisting exclusively of food eggs supplied by the females, makes the species difficult to propagate (Heselhaus, 1992 in WCMC, IUCN/SSC, and TRAFFIC, 1999). It is unclear whether this also applies to O. sylvatica. At the 15th Meeting of the CITES Committee in 1999 concerns were raised about the status of D. histrionicus in Ecuador, the basis for Non Detriment Findings and about captive breeding and exports (AC15 Proceedings). REFERENCES: Coloma, L. A., Guayasamin, J. M., and Menéndez-Guerrero, P. (2013). Lista Roja de Anfibios de Ecuador. Quito, Ecuador: AnfibiosWebEcuador, Fundación Otonga. URL: http://anfibioswebecuador.ec/listaroja/listaroja_spp.aspx?Id=176 Accessed: 23/10/2013. Coloma, L. A., Ron, S., Grant, T., and Lotters, S. (2004). Oophaga sylvatica. In: IUCN Red List of Threatened Species. Version 2013.1. URL: www.redlist.org Accessed: 20/09/2013. Hamilton, P., Mouette, C., and Almendariz, A. (2005). Análisis Inicial de la Herpetofauna en Bosques Secos y Húmedos de la Costa de Ecuador (p. 17). Reptile Research, Tucson. Ministerio del Ambiente. (2008). Situación actual del tráfico ilegal de la vida silvestre (p. 52). Dirección Nacional de Biodiversidad Unidad de Vida Silvestre. Ministerio del Ambiente. (2011). Manual para exportación de flora y fauna silvestre en el Ecuador (p. 26). Dirección Nacional de Biodiversidad Unidad de Vida Silvestre. Ministerio del Ambiente. (2012). Oficio Nro. MAE-DNB-2012-0408: Exportación ilegal de anfibios. Dirección Nacional de Biodiversidad. Ortega-Andrade, H. M., Bermingham, J., Aulestia, C., and Paucar, C. (2010). Herpetofauna of the Bilsa Biological Station, province of Esmeraldas, Ecuador. Check List, 6(1), 119–154. Ortiz, D. A., Coloma, L. A., and Frenkel, C. (2013). Oophaga sylvatica. In S. R. Ron, J. M. Guayasamin, M. H. Yanez-Munoz, and A. Merino-Viteri (Eds.), AmphibiaWebEcuador Version 2013.1. Museo de Zoología, Pontificia Universidad Católica del Ecuador. URL: http://zoologia.puce.edu.ec/vertebrados/anfibios/FichaEspecie.aspx?Id=1261 Accessed: 23/09/2013.

Oophaga sylvatica

Republic of Ecuador. (2003). Decreto No 3.516 - Biodiversidad (Libro IV, Títulos I a VII, del Texto Unificado de la Legislación Secundaria del Ministerio del Ambiente). WCMC, IUCN/SSC, and TRAFFIC. (1999). Review of significant trade in animal species included in CITES Appendix II: Detailed reviews of 37 species (Vol. Doc. AC 15). Cambridge, UK: World Conservation Monitoring Centre, IUCN Species Survival Commission and TRAFFIC Network.

Annex I: Key to purpose and source codes

Annex I: Key to purpose and source codes 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

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