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Page 1: Review of selected species subject to long- standing import … · 2016-10-20 · Review of selected species subject to long-standing import suspensions. Part IV. Prepared for The

UNEP-WCMC technical report

Review of selected species subject to long-

standing import

suspensions. Part IV.

(Version edited for public release)

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Review of selected species subject to long-standing import suspensions. Part IV.

Prepared for The European Commission, Directorate General Environment, Directorate E - Global & Regional

Challenges, LIFE ENV.E.2. – Global Sustainability, Trade & Multilateral Agreements, Brussels, Belgium

Prepared September 2016

Copyright European Commission 2016

Citation UNEP-WCMC. 2016. Review of selected species subject to long-standing import suspensions. Part IV.

UNEP-WCMC, Cambridge.

The UNEP World Conservation Monitoring Centre (UNEP-WCMC) is the specialist biodiversity

assessment of the United Nations Environment Programme, the world’s foremost intergovernmental

environmental organization. The Centre has been in operation for over 30 years, combining scientific

research with policy advice and the development of decision tools.

We are able to provide objective, scientifically rigorous products and services to help decision-makers

recognize the value of biodiversity and apply this knowledge to all that they do. To do this, we collate

and verify data on biodiversity and ecosystem services that we analyze and interpret in comprehensive

assessments, making the results available in appropriate forms for national and international level

decision-makers and businesses. To ensure that our work is both sustainable and equitable we seek to

build the capacity of partners where needed, so that they can provide the same services at national and

regional scales.

The contents of this report do not necessarily reflect the views or policies of UNEP, contributory

organisations or editors. The designations employed and the presentations do not imply the expressions

of any opinion whatsoever on the part of UNEP, the European Commission or contributory

organisations, editors or publishers concerning the legal status of any country, territory, city area or its

authorities, or concerning the delimitation of its frontiers or boundaries. The mention of a commercial

entity or product in this publication does not imply endorsement by UNEP.

UNEP World Conservation Monitoring Centre

(UNEP-WCMC)

219 Huntingdon Road,

Cambridge CB3 0DL, UK

Tel: +44 1223 277314

www.unep-wcmc.org

UNEP promotes

environmentally sound

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sustainable forests and

recycled fibre is encouraged.

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Contents

Introduction and summary………………………………………………………………………………………………………………4

Cervus elaphus bactrianus II/B ..............................................................................................................5

Hexaprotodon liberiensis II/B ............................................................................................................... 8

Ateles fusciceps II/B .............................................................................................................................. 12

Lagothrix lagotricha II/B ...................................................................................................................... 16

Lagothrix lugens II/B ............................................................................................................................ 22

Lagothrix poeppigii II/B ........................................................................................................................ 25

Lophocebus albigena II/B ..................................................................................................................... 31

Piliocolobus badius II/B ........................................................................................................................34

Gyps bengalensis II/B ............................................................................................................................43

Bugeranus carunculatus II/B ............................................................................................................... 52

Agapornis nigrigenis II/B ..................................................................................................................... 56

Gopherus agassizii II/B ......................................................................................................................... 61

Appendix ............................................................................................................................................... 65

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Introduction

This document provides reviews of 42 taxon/country combinations of taxa currently subject to long-standing Article 4.6(b) import suspensions. The document is provided to inform discussions by the Scientific Review Group as to whether these trade restrictions may still be warranted.

Forty two taxon/country combinations are presented in this report. Trade data were downloaded on

03/08/20161.

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

Introduction and summary

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Cervus elaphus bactrianus

ARTIODACTYLA: CERVIDAE

Cervus elaphus bactrianus II/B

Taxonomic note

Cervus elaphus bactrianus is listed in CITES Appendix II. However, the CITES Standard reference,

(Wilson and Reeder, 2005) considers C. e. bactrianus to be a synonym of C. e. yarkandensis.

Lorenzini and Garofalo (2015) suggested that Tarim red deer from Central Asia, including

C. e. yarkandensis, C. e. bactrianus and C. e. hanglu should be recognised as Cervus hanglu. For the

purposes of this review, the name Cervus elaphus bactrianus is used.

Trade patterns

Cervus elaphus bactrianus was listed in Appendix II on 01/07/1975 and in Annex B of the EU Wildlife

Trade Regulations on 01/06/1997.

Uzbekistan has submitted annual reports for the years 2006-2014, but has not yet submitted an annual

report for 2015. Uzbekistan published annual export quotas for two trophies of C. e. bactrianus in 2010,

three trophies in 2012 and 2013 and six trophies in 2016.

There was no direct or indirect trade in C. e. bactrianus from Uzbekistan to the EU-28 or countries other

than the EU-28 reported over the period 2006-2015. Prior to 2006 the only reported trade was two

captive-bred trophies exported for hunting purposes in 2000, as reported by Uzbekistan.

SYNONYMS: Cervus elaphus yarkandensis

COMMON NAMES: Bokharan Deer (EN), Ciervo del Turquestán (ES), Cerf élaphe du Turkestan (FR)

RANGE STATES: Afghanistan, Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan

UNDER REVIEW: Uzbekistan

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Uzbekistan first applied on 30/04/2004 and last confirmed on 28/05/2015.

IUCN: Not Assessed (Assessed as Least Concern at the species level)

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Cervus elaphus bactrianus

Conservation status

Cervus elaphus bactrianus is a deer that was reported to occur in the riparian forests of the Amudaria,

Zaravshan, Ily and Syrdaria river valleys of south-west Tajikistan, north-east Turkmenistan and east and

south-east Uzbekistan (CMS, 2011). C. e. bactrianus was reported to primarily inhabit riparian (Tugay)

forests (Pereladova, 2013; Safarov et al., 2014; Vagg, 2015). Within good habitat conditions, it was

believed to be unusual for C. e. bactrianus to migrate, however, 30-50 per cent of the population were

estimated to migrate seasonally across national borders in search of better habitats (CMS, 2016a).

Cervus elaphus (which has a wide circumpolar distribution) has been assessed as Least Concern by the

IUCN (Lovari et al., 2008). The subspecies (C. e. bactrianus) has not been assessed by the IUCN,

although it is listed in the Red Data Books of all range countries (CMS, 2011). In 2010, the population was

estimated at 1600 individuals in Kazakhstan, Tajikistan, Turkmenistan and Uzbekistan; there was no

information on the population status in Afghanistan (CMS, 2011). The population was thought to have

stabilised or be increasing in the range countries (CMS, 2011; Pereladova, 2013; Ministry of Nature

Protection of Turkmenistan, 2014; Ministry of Environment and Water Resources of the Republic of

Kazakhstan, 2015).

C. e. bactrianus is threatened by habitat destruction, alteration of local water systems, and illegal

hunting (Wilson and Mittermeier, 2011; Vagg, 2015). High levels of habitat fragmentation was noted to

prevent natural range expansion (CMS, 2011).

The species is listed on Appendix I of the Convention on the Conservation of Migratory Species of Wild

Animals (CMS) and there is a Memorandum of Understanding (MoU) in place covering Kazakhstan,

Tajikistan, Turkmenistan and Uzbekistan (Vagg, 2015; CMS, 2016b). The MoU provides an

intergovernmental framework for governments, scientists and other stakeholders to monitor and

coordinate ongoing conservation efforts (Vagg, 2015). In addition, an action plan has been established,

aiming to, inter alia, restore the range and number of suitable habitats for the subspecies (CMS, 2002).

Mallon (2013) reported trophy hunting of C. e. bactrianus was possible in one hunting reserve in

Kazakhstan under strict regulation. C. e. bactrianus was listed on the list of priority species of the Large

Herbivore Initiative, founded in 1988 by WWF International (Baerselman, 2002). This initiative funded a

project of protected areas, ranger patrols and captive breeding which reportedly led to a slow recovery of

the subspecies (Baerselman, 2002).

Uzbekistan: Cervus elaphus bactrianus has been recorded in eastern and south-eastern Uzbekistan

(Mallon and Kingswood, 2001; CMS, 2011).

C. e. bactrianus is listed in the Red Data Book of Uzbekistan, where it has been assessed as ‘endangered’

(Azimov et al., 20092). In 2015, C. e. bactrianus populations were reported to be declining in Uzbekistan

(Sadikov et al., 2015), while they had been increasing between 1999 and 2011 (Pereladova, 2013). In 2010

there were an estimated 900 individuals in Uzbekistan (CMS, 2011); the population had previously been

estimated at 300 individuals (Azimov et al., 2009).

Uzbekistan is signatory of the CMS Bukhara Deer MoU and the CMS Action Plan for the species, which

included, inter alia, financial support for reserves, reintroduction of the species, assessment of habitat

availability and increased connectivity and establishment of reserves (CMS, 2002). Uzbekistan

(Zarafshan Reserve) was the site of the first reintroduction of the species in 2005 (Pereladova, 2013).

2 Reference translated using Google translate.

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Cervus elaphus bactrianus

The subspecies was reported to occur in three protected areas in Uzbekistan: the Surkhan National

Reserve [eastern Uzkeistan], Kyzylkum Nature Reserve [eastern Uzkekistan] and Zarafshan Nature

Reserve [south-eastern Uzbekistan] (CMS, 2011).

Mallon (2013) noted that trophy hunting of C. e. bactrianus was “theoretically possible” in Badai-tugai

but Pereladova (2013, in litt. to Mallon 2013) noted that overcoming legal regulations was very

complicated.

The Regulations on Hunting and Fishing on the territory of the Republic of Uzbekistan (2010) govern

hunting regulations (Ministry of Justice, 2010 in Mallon, 2013). Hunting of species listed on the Red Data

Book of Uzbekistan is permitted with species dispensation from the Council of Ministers (Mallon, 2013).

No further information on the status, population size, threats or management of the species in

Uzbekistan could be identified.

References

Azimov, J.A., Umarov, N.M., Mirabdullayev, I.M., Khamrayev, A.Sh., Mirzayev, U.T., Chikin,YU.A., Lanovenko, E.N., and Mitropolskaya, Y.O. 2009. The Red Data Book of the Republic of Uzbekistan, Volume II Animals. Chinor ENK. 218 pp. [Translated using Google translate]

Baerselman, F. 2002. The Large Herbivore Initiative: An Eurasian conservation and restoration programme for a key species group in ecosystems (Europe, Russia, Central Asia and Mongolia). In: Pasture Landscapes and Nature Conservation. 303–312.

CMS 2002. Action Plan concerning Conservation and Restoration of the Bukhara Deer (Cervus elaphus bactrianus). 12 pp.

CMS 2011. First meeting of the signatories to the memorandum of understanding concerning conservation and restoration of the bukhara deer (Cervus elaphus bactrianus). NEP/CMS/BKD1/Doc.6. CMS Secretariat, Bergen, Norway. 17 pp.CMS 2016a. Cervus elaphus yarkandensis. Available at: http://www.cms.int/en/species/cervus-elaphus-yarkandensis. [Accessed: 19 September 2016]

CMS 2016b. Bukhara Deer, CMS. Available at: http://www.cms.int/bukhara-deer/legalinstrument/bukhara-deer. [Accessed: 1 August 2016].

Lorenzini, R. and Garofalo, L. 2015. Insights into the evolutionary history of Cervus (Cervidae, tribe Cervini) based on Bayesian analysis of mitochondrial marker sequences, with first indications for a new species. Journal of Zoological Systematics and Evolutionary Research, 53(4): 340–349.

Lovari, S., Herrero, J., Conroy, J., Maran, T., Giannatos, G., Stubbe, M., Aulagnier, S., Jdeidi, T., Masseti, M., Nader, I. et al. 2008. Cervus elaphus. The IUCN Red List of Threatened Species 2016. Available at: http://www.iucnredlist.org. [Accessed: 1 August 2016].

Mallon, D.P. and Kingswood, S.C. 2001. Antelopes. Part 4: North Africa, the Middle East, and Asia. Global Survey and Regional Action Plans. SSC Antelope Specialist Group.IUCN, Gland, Switzerland and Cambridge, UK. 260 pp.

Mallon, D. 2013. Trophy hunting of CITES-listed species in central Asia. Secretariat of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), Geneva, Switzerland. pp.48

Ministry of Environment and Water Resources of the Republic of Kazakhstan 2015. The fifth national report on progress in implementation of the Convention on Biological. Ministry of Environment and Water Resources of the Republic of Kazakhstan, Kazakhstan. 140 pp.

Ministry of Nature Protection of Turkmenistan 2014. Turkmenistan Fifth National report on the implementation of the Convention on Biological Diversity. The Ministry of Nature Protection of Turkmenistan. 33 pp [Translated using Google translate]

Pereladova, O. 2013. Restoration of Bukhara deer (Cervus elaphus bactrianus Lydd.) in Central Asia in 2000-2011. Deer Specialist Group News, 25: 19–30.

Sadikov, K., Abdurahmanov, A. and Bekmirzaeva, I. 2015. Fifth national report of the Republic of Uzbekistan on conservation of biodiversity. UNDP Uzbekistan. 62 pp.

Safarov, N., Novikova, T. and Shermatov, K. 2014. Fifth National report on preservation of biodiversity of the Republic of Tajikistan. National Center on Biodiversity and Biosafety of the Republic of Tajikistan, Dushanbe, Tajikistan. 148 pp.

Vagg, R. 2015. CMS family guide: the encyclopaedia of the Convention on the Conservation of Migratory Species of Wild Animals. Bonn, Germany. 1-26 pp.

Wilson, D.E. and Mittermeier, R.A. 2011. Handbook of the Mammal of the world - Vol. 2. Hoofed Mammals. Lynx Edicions, Barcelona. 886 pp.

Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed.

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Cervus elaphus bactrianus

The John Hopkins University Press, Baltimore, USA. 2142 pp.

MAMMALIA: HIPPOPOTAMIDAE

Hexaprotodon liberiensis II/B

Taxonomic note

The current CITES Standard Reference (Wilson and Reeder, 2005) recognises two subspecies,

Hexaprotodon liberiensis liberiensis and Hexaprotodon liberiensis heslopi. A review of the taxonomy and

phylogeny of the Hippopotamids by Boisserie (2005) restricted the definition of Hexaprotodon to a fossil

lineage and revalidated Choeropsis for the Pygmy Hippopotamus. Although a number of recent sources

accept this classification, this review refers to the species as H. liberiensis in accordance with the

Standard Reference (Wilson and Reeder, 2005).

Trade patterns

Hexaprotodon liberiensis was listed in Appendix II on 01/07/1975 and in Annex B of the EU Wildlife

Trade Regulations on 01/06/1997.

Nigeria has submitted annual reports for the years 2006-2009 and 2012 but has not yet submitted annual

reports for 2010-2011 or 2013-2015. Nigeria has never published an annual export quota for H. liberiensis.

There has never been any reported direct or indirect trade in H. liberiensis originating from Nigeria to

the EU-28 or elsewhere.

SYNONYMS: Choeropsis liberiensis

COMMON NAMES: Pygmy Hippopotamus (EN), Hippopotame Pygmée (FR), Hipopótamo Pigmeo (ES)

RANGE STATES: Côte d'Ivoire, Guinea, Guinea Bissau (distribution uncertain), Liberia, Nigeria (extinct), Sierra Leone

UNDER REVIEW: Nigeria

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

Current no opinion iii) for wild specimens from Côte d'Ivoire and Sierra Leone formed on 18/05/2010. Current no opinion iii) for wild specimens from Guinea formed on 14/09/2010.

Current no opinion i) for wild specimens from Guinea Bissau formed on 18/05/2010.

IUCN: Endangered

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Hexaprotodon liberiensis

Conservation status

Hexaprotodon liberiensis is a small hippopotamus endemic to West Africa, where the nominate

subspecies was reported to be restricted to lowland forests of Côte d’Ivoire, Sierra Leone, Liberia and

Guinea (Robinson, 2013). The second subspecies, H. l. heslopi, was known only from the Niger Delta,

Nigeria, but there have been no reliable reports of the subspecies since 1945 and it was considered

probably extinct (Robinson, 2013). According to Mallon et al. (2011), the most recent records of the

species were from protected areas.

The species was noted to have a gestation period of six to seven months in captivity (Zschokke and

Steck, 2001) and individuals reportedly reach reproductive maturity between three and five years of age

(Lang, 1975).

H. liberiensis was categorised as Endangered by the IUCN on the basis of a continuing population

decline over two generations, based on estimates of habitat loss across the species range, coupled with

an increase in hunting intensity (Ransom et al., 2015). Recent assessments concluded that the total

population size of the species was unknown (Robinson, 2013; Ransom et al., 2015). In the early 1990s, it

was estimated to be up to a few thousand (Eltringham, 1993) and was considered by Robinson (2013)

probably larger than this. The species’ range was reported to have “declined dramatically” in the past 100

years (Robinson, 1971), but most acutely in the past 50 (Robinson, 2013). The remaining populations

were reported to be fragmented across the species’ range (Eltringham, 1993; Ransom et al., 2015).

The main threats to the species were reported to include habitat fragmentation, land conversion and

hunting (Mallon et al., 2011; Robinson, 2013; Ransom et al., 2015). According to Ransom et al. (2015),

H. liberiensis are taken opportunistically by bushmeat hunters, although not specifically targeted for

subsistence hunting. Ransom et al. (2015) also noted reports from some areas of the species being

targeted by commercial hunters.

A conservation strategy action plan for H. liberiensis was published in 2011 (Mallon et al., 2011).

While the species was reported to be legally protected in every range state, levels of enforcement were

considered limited (Ransom et al., 2015).

Nigeria: The only reported occurrence of Hexaprotodon liberiensis in Nigeria was for the endemic

subspecies H. l. heslopi, found only in the Niger Delta (Robinson, 2013); there have been no reliable

reports of the subspecies since 1945 and it was considered probably extinct (Anadu, 1987; Eltringham,

1993; Mallon et al., 2011; Robinson, 2013), including in the species’ 2015 IUCN Red List assessment

(Ransom et al., 2015).

H. l. heslopi was reported to formerly have occurred approximately 1800 km east of the range of

H. l. liberiensis, from the Niger Delta east to the Cross River of Nigeria (Heslop, 1945 in Robinson, 2013).

The subspecies was known only from reports from the 1930s and 1940s (Heslop, 1945 in Robinson, 2013;

Corbet, 1969) from the swamps of the Cross River region of Calabar Province [eastern Nigeria] and the

swamps of the Niger River and its tributaries in the [former] British colonial administrative divisions of

Kwale, Asaba, Onitsha and Aboada (Robinson, 2013) and from anecdotal reports (Mallon et al., 2011).

Locations where the species was reported to have been seen or shot included: Aboh, Akpede, Akunomi,

Biseni, Ikibiri, Isemu, Lalagbene, Odi, Omoku and Sabagreia on the Nun River between Kaiama and

Yenagoa [all located in southern Nigeria] (Powell, 1993 in Eltringham, 1999). Heslop (1945 in Eltringham,

1999) was reported to have estimated the total population size as 30 individuals, with the largest

subpopulation consisting of seven individuals. In a review of reported sightings by hunters, Blench

(2007) noted that the consensus was that the subspecies became “practically” extinct in the 1960s in

some areas, with a few reports of sightings in the early 1990s considered consistent with lone vagrant

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Hexaprotodon liberiensis

individuals in the Odi-Sampou area [southern Nigeria]. Hamadina et al. (2007 in Hamadina and

Anyanwu, 2012), reported that experienced hunters on the Wilberforce Island of the Niger Delta

[southern Nigeria] stated that H. liberiensis would visit the area up to the 1970s. In 1993, Oates (in litt. to

Eltringham, 1993) suggested that H. l. heslopi may still occur in the Niger Delta, on the basis that

residents still knew of the species. Blench (2007) also noted local reports of the species from south-east

of Tungbo and the Upper Orashi Forest Reserve [southern Nigeria], although these were reported to be

based largely on sightings of tracks or evidence of disturbance.

Although it was considered very unlikely that any individuals remain, it was noted that a final effort to

investigate may be worthwhile (Mallon et al., 2011).

The species was listed as Endangered (Schedule 1: Endangered Species of Animals in Relation to which

International Trade is Absolutely Prohibited) in the Nigerian Endangered Species Decree No 11 of 1985

and the revised edition, the Endangered Species (Control of International Trade and Traffic) Act, 2013,

which prohibits their trade and makes it an offence to hunt or capture them (Government of Nigeria,

1985; 2013). According to Flacke et al. (2015), only one published account of the species management in

captivity in Nigeria (Jos Wildlife Park) exists.

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Hexaprotodon liberiensis

References

Anadu, P.A. 1987. Progress in the conservation of Nigeria’s wildlife. Biological Conservation, 41: 237–251.

Blench, R. 2007. Mammals of the Niger Delta, Nigeria. Unpublished. 75 pp.

Boisserie, J.R. 2005. The phylogeny and taxonomy of Hippopotamidae (Mammalia: Artiodactyla): a review based on

morphology and cladistic analysis. Zoological Journal of the Linnean Society, 143(1): 1–26.

Corbet, G.B. 1969. The taxonomic status of the Pygmy hippopotamus, Choeropsis liberiensis, from the Niger Delta.

Journal of Zoology, 158: 387–394.

Eltringham, S.K. 1999. The Hippos. Academic Press, London. 184 pp.

Eltringham, S.K. 1993. The Pygmy Hippopotamus (Hexaprotodon liberiensis). In: Oliver, W. (Ed.). Status Survey and

Conservation Action Plan: Pigs, Peccaries, and Hippos. IUCN, Gland, Switzerland. 55–60.

Flacke, G.L., Chambers, B.K., Martin, G.B. and Paris, M.C.J. 2015. The Pygmy Hippopotamus Choeropsis liberiensis

(Morton, 1849): Bringing to light research priorities for the largely forgotten, smaller hippo species. Der

Zoologische Garten, 84(5–6): 234–265.

Government of Nigeria 2013. Endangered Species (Control of International Trade and Traffic) Act. Revised edition of

Decree No. 11 of 1985.

Government of Nigeria 1985. Endangered Species (Control of International Trade and Traffic) Act (1985 No. 11).

Hamadina, M.K. and Anyanwu, D.I. 2012. A cursory review of the consequences of human activities and land-use

changes in the Niger Delta. Research Journal of Environmental and Earth Sciences, 4(5): 597–604.

Hamadina, M.K., Otobotekere, D. and Anyanwu, D.I. 2007. Impact assessment and biodiversity considerations in

Nigeria: A case study of Niger Delta University campus project on wildlife in Nun River Forest Reserve.

Management of Environmental Quality, 18(2): 179–197.

Heslop, I.R.P. 1945. The pygmy hippopotamus in Nigeria. Field (Nigeria), 185: 629–630.

Lang, E.M. 1975. Das Zwergflußpferd Choeropsis liberiensis. A. Ziemsen Verlag, Wittenberg Lutherstadt. 63 pp.

Mallon, D., Wightman, C., De Ornellas, P. and Ransom, C. 2011. Conservation Strategy for the Pygmy Hippopotamus.

IUCN Species Survival Commission, Gland, Switzerland and Cambridge, UK. 48 pp.

Powell, C.B. 1993. Sites and Species of Conservation Interest in the Central Axis of the Niger Delta. Nigeria

(Unpublished Report).

Ransom, C., Robinson, P.T. and Collen, B. 2015. Choeropsis liberiensis. The IUCN Red List of Threatened Species

2015. Available at: www.iucnredlist.org. [Accessed: 19 November 2016].

Robinson, P.T. 2013. Choeropsis liberiensis Pygmy Hippopotamus. In: Kingdom, J. and Hoffman, M. (Eds.). Mammals

of Africa. Volume VI: Pigs, Hippopotamuses, Chevrotain, Giraffes, Deer and Bovids. Bloomsbury Publishing,

London, UK. 704.

Robinson, P.T. 1971. Wildlife trends in Liberia and Sierra Leone. Oryx, 11(2–3): 117–122.

Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed.

The John Hopkins University Press, Baltimore, USA. 2142 pp.

Zschokke, S. and Steck, B. 2001. Tragzeit und Geburtsgewicht beim Zwergflußpferd, Hexaprotodon liberiensis.

Zoologische Garten, 71(1): 57–61.

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Ateles fusciceps

PRIMATES: ATELIDAE

Ateles fusciceps II/B

Taxonomic note

Whilst the CITES Standard Reference (Wilson and Reeder, 2005) recognises two subspecies, A. fusciceps

fusciceps and A. fusciceps rufiventris (and considers A. f. dariensis and A. f. robustus to be synonyms of

A. f. rufiventris), the taxonomy of Ateles fusciceps has been subject to debate in the literature (Rylands et

al., 2006; Morales Jiménez, 2007).

For the purposes of this review, the taxonomy accepted by the CITES Standard Reference is followed,

but for clarification, the nomenclature used in the cited source is given in square brackets.

Trade patterns

Ateles fusciceps was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

There has never been any reported trade in A. fusciceps from Colombia or Panama to the EU-28 or

elsewhere. These countries have also never published export quotas for the species.

Ecuador: Ecuador has submitted annual reports for the years 2007-2014, but has not yet submitted

annual reports for 2006 or 2015. Ecuador has never published an annual export quota for A. fusciceps.

There was no direct or indirect trade in A. fusciceps from Ecuador to the EU-28 or elsewhere reported

over the period 2006-2015. Prior to 2006, the only reported trade was three wild-sourced specimens

directly exported to countries other than the EU-28 for scientific purposes in 2002, as reported by

Ecuador.

SYNONYMS: Ateles geoffroyi fusciceps, Ateles geoffroyi rufiventris

COMMON NAMES: Brown-headed Spider Monkey (EN), Atèle à Tête Brune (FR), El Mono Araña de Cabeza Marrón (ES)

RANGE STATES: Colombia, Ecuador, Panama

UNDER REVIEW: Colombia, Ecuador, Panama

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Colombia, Ecuador and Panama first applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Critically Endangered

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Ateles fusciceps

Conservation status

Ateles fusciceps occurs in Ecuador, Panama and Colombia; the subspecies A. fusciceps fusciceps was

noted to occur in north-west Ecuador and A. f. rufiventris in eastern Panama and western Colombia

(Mittermeier et al., 2013). A. f. fusciceps was reported to occur in tropical lowland and subtropical forests

at altitudes between 100 and 1700 m above sea level, and A. f. rufiventris in dry, humid and cloud forests

up to altitudes of 2000 to 2500 m above sea level (Mittermeier et al., 2013).

A. fusciceps was noted to require large areas of continuous primary forest (Defler, 2004 in Peck et al.,

2011). The species reportedly has an inter-birth interval of two to three years and its low reproductive

rate was considered to hinder the ability of the species to recover from population declines (Ross and

Jones, 1999; Tirira, 2007 in Peck et al., 2011). Individuals were noted to live up to 24 years of age

(Mittermeier et al., 2013).

A. fusciceps was categorised by the IUCN as Critically Endangered due to its small population size,

restricted distribution and pressure facing populations (Cuarón et al., 2008; Tirira, 2001 in Peck et al.,

2011). The population size was considered to be declining (Cuarón et al., 2008) and was believed to be in

the low hundreds (Mittermeier et al., 2013).

Hunting was considered one of the major pressures facing A. fusciceps (Peck et al., 2011). Bushmeat was

noted to be the main reason for hunting, with the pet trade to a lesser extent (Altherr, 2007).

Colombia: A. f. rufiventris was reported to occur in the Chocó region (Mittermeier et al., 2013) in west

Colombia (Defler et al., 2003; Mittermeier et al., 2013), where it was reported from the middle Baudó

(Defler et al., 2003). In the Chocó region, the subspecies was said to be known only from Las Orquídeas

and Los Katíos National Natural Parks (Mittermeier et al., 2013). The presence of the subspecies

A. f. fusciceps in Colombia was considered uncertain and a record from Barbacoas, Narino Department

was considered unconfirmed (Mittermeier et al., 2007).

A. fusciceps [A. geoffroyi rufiventris] was categorised as ‘endangered’ in Colombia in 2001 (Defler et al.,

2003) and 2010 (Ministerio de Ambiente, 2010). The population in Los Katíos National Natural Park was

believed to be small and possibly declining (Mittermeier et al., 2013).

Habitat fragmentation and destruction, and hunting were considered threats to Ateles in Colombia, and

A. fusisceps [A. geoffroyi rufiventris] was reportedly heavily hunted (Defler et al., 2003). Colombian law

reportedly permits subsistence hunting by indigenous people within protected areas, whilst commercial

hunting is illegal (PNNA, 2006 in Parathian and Maldonado, 2010).

Ecuador: A. f. fusciceps was noted to be the only subspecies occurring in Ecuador and was considered to

be restricted to two locations: the Awá Ethnological Reserve, near the border with Colombia and the

Cotacachi-Cayapas Ecological Reserve and its buffer zone, which includes Los Cedros protected forest

[north-western Ecuador] (Mittermeier et al., 2007; 2013). As such, most of its area of occurrence was

reported to be within protected areas (Tirira, 2004). Mittermeier et al. (2013) noted that A. f. fusciceps

historically ranged “from the Colombian border south to the Cordillera de Colonche in Guaya Province”

[south-western Ecuador].

Tirira (2004) estimated the wild population of A. fusciceps in Ecuador to be fewer than 250 individuals

and noted that no subpopulation exceeded 25 reproductive pairs or 50 mature individuals. The

population was considered to be decreasing (Cuarón et al., 2008). The species was previously considered

to be “widely distributed in tropical forests” (Rylands et al., 1997 in Altherr, 2007) but it was noted to

have become locally extinct in several areas including the whole central coast of Ecuador, the forests of

Ríos Cayapas, San Miguel, Ónzole and Santiago in Esmereldas Province [north-western Ecuador] (Tirira,

2004).

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Gavilanez-Endara, (2006 in Peck et al., 2011) reported a population density of 1.16 individuals/km2 of

A. fusciceps at the Los Cedros Biological Reserve. In 2007, Peck et al., (2011) estimated the population

density of A. fusciceps to be 0.9 individuals/km2 in Los Cedros Biological Reserve, 3.76 individuals/km2

in Santa Rosa de Naranjal, 0.57 individuals/km2 in Leon Febres Cordero [all forests to the south-west of

Cotacachi-Cayapas Ecological Reserve] and 7.49 individuals/km2 in Tesoura Escondida [forest to the

west of Cotacachi-Cayapas Ecological Reserve]. Peck et al. (2011) noted that high levels of hunting were

suspected at Leon Febres Cordero and that the population density at sites under low hunting pressure

varied with altitude. Between 2013 and 2015, Salcedo et al. (2015) carried out population density surveys

of A. f. fusciceps and estimated a density of 3.49 individuals/km2 in Pambilar Wildlife refuge [a protected

area in north-western Ecuador], and a density between 9.5 and 22 individuals/km2 in Tesoro Escondido

[north-western Ecuador]. Rapid assessment surveys, also carried out between 2013 and 2015, confirmed

the presence of the subspecies in Santa Rosa del Naranjal and Cotacachi-Cayapas Ecological Reserve, but

not in four survey sites in Pichincha province (Salcedo et al., 2015).

In 2008, the IUCN categorised the Ecuadorian endemic A. f. fusciceps as Critically Endangered, as the

population was estimated to have declined by more than 80 per cent over the past 45 years (Cuarón et

al., 2008). The species was listed on the red list of mammals for Ecuador in 2001 (Tirira, 2001 in

Mittermeier et al., 2007) and A. f. fusciceps was included in the 2011 national red list as ‘critically

endangered’ (Tirira, 2011).

Deforestation and hunting were considered to be the main threats to the species in Ecuador (Tirira et

al., 2012).

Resolution No. 105 Ministry of the Environment prohibits hunting and commercial use of A. fusciceps

throughout Ecuador (Ministerio del Ambiente, 2000). Tirira (2004) noted that long-term conservation of

the species may not be guaranteed in Awá Ethnological Reserve, as indigenous people are free to use the

resources within the reserve.

Panama: The subspecies A. f. rufiventris was reported to occur in Bayano [central-eastern Panama],

Turia [eastern Panama], Serranía del Maja [eastern Panama], Darién National Park [eastern Panama,

near the border with Colombia], San Blas [north-eastern Panama], Tacrcuna [eastern Panama, near the

border with Colombia]. Mittermeier et al. (2013) noted that the species may also occur in Chagres and

Darién National Parks.

The populations of A. f. rufiventris were reportedly fragmented and a survey by means of a questionnaire

indicated that the population may be between 250 and 2500 individuals (Matamoros and Seal, 2001).

A. fusciceps was categorised as ‘vulnerable’ in Panama in 2008 (República de Panamá, 2008) and was

considered to be threatened by subsistence hunting, human interference and loss of habitat (Matamoros

and Seal, 2001).

References

Altherr, S. 2007. Going to pot. The neotropical bushmeat crisis and its impact on primate populations. Munich. 1-27 pp.

Cuarón, A.D., Morales, A., Shedden, A., Rodríguez-Luna, E. and de Grammont, P.C. 2008. Ateles fusciceps ssp. fusciceps. The IUCN Red List of Threatened Species 2008: Available at: http://www.iucnredlist.org/. [Accessed: 28 September 2016].

Defler, T.R. 2004. Primates of Colombia. Conservation International, Washington DC. Defler, T.R., Rodríguez-M, J. V. and Hernández-Camacho, I.J. 2003. Conservation priorities for Colombian primates.

Primate Conservation, 19: 10–18. Gavilanez-Endara, M.M. 2006. Demografía, actividad y preferencia de hábitat de tres especies de primates (Alouatta

palliata, Ateles fusciceps y Cebus capucinus) en un bosque nublado del noroccidente ecuatoriano. Pontificia Universidad Católica del Ecuador, Quito.

Matamoros, Y. and Seal, U.S. 2001. Informe Final. Taller para la conservación asesoramiento y manejo planificado

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Ateles fusciceps

para los primates mesoamericanos, Parque Zoológico Simón Bolívar, San José, Costa Rica, 23-25 Junio 1997. IUCN/SSC Conservation Breeding Specialist Group (CBSG). Apple Valley, Minnesota, USA.

Ministerio del Ambiente 2000. Resolución No 105 - Regulación del control de cacería y vedas de especies de fauna silvestre en el territorio nacional.

Ministerio de Ambiente Vivienda y Desarrollo Territorial 2010. Resolución número 383, 23 de febrero de 2010. República de Colombia.

Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (Eds.) 2013. Handbook of the mammals of the world. Vol. 3 Primates. Lynx Edicions, Barcelona, Spain. 951 pp.

Mittermeier, R.A., Schwitzer, C., Rylands, A.B., Taylor, L. a, Chiozza, F., Williamson, E. a and Wallis, J. and Clark, F. E. 2012. Primates in peril: The world’s 25 most endangered primates 2012–2014. IUCN SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), and Bristol Zoological Society, Arlington, VA, USA. 87 pp.

Morales Jiménez, A.L. 2007. Action Plan of the spider monkeys Ateles hybridus and Ateles fusciceps in Colombia. Available at: http://s3.amazonaws.com/academia.edu.documents/3468945/Atelesactionplanweb.pdf?AWSAccessKeyId=AKIAJ56TQJRTWSMTNPEA&Expires=1473170930&Signature=e1rsyYRwnTMiLAhbn+jjOW79ssc=&response-content-disposition=inline; filename=Action_Plan_of_the_spider_monkeys_At. [Accessed 6 September 2016].

Parathian, H.E. and Maldonado, A.M. 2010. Human–nonhuman primate interactions amongst Tikuna people: perceptions and local initiatives for resource management in Amacayacu in the Colombian Amazon. American journal of Primatology, 72(10): 855–865

Peck, M., Thorn, J., Mariscal, A., Baird, A., Tirira, D. and Kniveton, D. 2011. Focusing conservation efforts for the critically endangered brown-headed spider monkey (Ateles fusciceps) using remote sensing, modeling, and playback survey methods. International Journal of Primatology, 32(1): 134–148.

PNNA. 2006. Línea base del Parque Nacional Natural Amacayacu. Leticia: Unidad Administrativa Especial del Sistema de Parques Nacionales Naturales (UAESPNN). 162p

República de Panamá 2008. Autoridad Nacional del ambiente (ANAM) Resolución No. AG - 0051-2008. Annex 1. Ross, C. and Jones, K.E. 1999. Socio-ecology and the evolution of primate reproductive rates. In: Lee, D.C. (Ed.).

Comparative primate socio-ecology. Cambridge University Press., Cambridge (UK). 73–110. Rylands, A.B., Groves, C.P. and Mittermeier, R.A. 2006. Taxonomy and Distributions of Mesoamerican Primates. 29–

79. Rylands, A.B., Mittermeier, R.A. and Rodriguez-Luna, E. 1997. Conservation of neotropical primates: threatened

species and an analysis of primate diversity by country and region. Folia primatologica, 68: 134–160. Salcedo, N.F., Cortes, F.A. and M, R.P. 2015. Participatory Conservation of the Critically Endangered Ecuadorian

Brown-Headed Spider Monkey. Proyecto Washu. Avalable at: http://www.conservationleadershipprogramme.org/media/2016/04/02154613_Ecuador_FinalReport_Participatory-Conservation-of-the-Critically-Endangered-Ecuadorian-Brown-Headed-Spider-Monkey_19thOct15.pdf [Accessed 6 September 2016]

Tirira, D. 2004. Estado actual del mono araña de cabeza café (Ateles fusciceps) (Primates: Cebidae) en el Ecuador. http://spidermonkey. zoodoue. fr/Estudio-Ateles-fusciceps.html, Available at: http://s3.amazonaws.com/academia.edu.documents/32277659/Tirira_2003-Estudio_actual_de_Ateles_fusciceps_en_Ecuador.pdf?AWSAccessKeyId=AKIAJ56TQJRTWSMTNPEA&Expires=1468844418&Signature=lEN6ZPA+hbbyAAULeW7NoLOwZiI=&response-content-disposition=inline; [Accessed: 18 July 2016].

Tirira, D. 2007. Guía de Campo de los Mamíferos del Ecuador. Ediciones Murciélago Blanco, Quito (Ecuador). Tirira, D. 2001. Libro Rojo de los Mamíferos del Ecuador. SIMBIOE, EcoCiencia, Ministerio del Ambiente y UICN,

Quito. Tirira, D.G., Morales-Jiménez, A.L. and Moscoso-R., P. 2012. Ecuadorian brown-headed spider monkey. In: Primates

in peril: The world’s 25 most endangered primates 2012-2014. 75–76. Tirira, D.G. 2011. Libro rojo de los mamíferos del Ecuador. 2a. edició. Fundación Mamíferos y Conservación, Pontificia

Universidad Católica del Ecuador y Ministerio del Ambiente del Ecuador. Publicación especial sobre los mamíferos del Ecuador 8. Quito. 383-386 pp.

Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed.

The John Hopkins University Press, Baltimore, USA. 2142 pp.

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Lagothrix lagotricha

PRIMATES: ATELIDAE

Lagothrix lagotricha II/B

Taxonomic note

The taxonomy of Lagothrix lagotricha was revised by Groves (2001 in Mittermeier et al., 2013), elevating

the subspecies L. l. lagotricha, L. l. lugens, L. l poeppigii and L. l. cana to species level. The CITES

Standard Reference (Wilson and Reeder, 2005) reflects this nomenclature.

For the purposes of this review, the nomenclature accepted by the CITES Standard Reference is

followed, but for clarification, the nomenclature used in the literature is given in square brackets. For

example, some sources continue to recognise some or all of the species as subspecies of L. lagotricha

(Mittermeier et al., 2013; Defler, 2003; Dew, 2005) and older sources may refer to L. lagotricha without

specifying the subspecies; in these instances, the information has been included in the L. lagotricha

review unless there is a reason to suggest it refers to L. lugens, L. poeppigii or L. cana.

Trade patterns

Lagothrix lagotricha was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

Brazil: Brazil has submitted annual reports for the years 2006-2014, but has not yet submitted an annual

report for 2015. Brazil has never published an annual export quota for L. lagotricha.

Direct exports of L. lagotricha from Brazil to the EU-28 2006-2015 comprised live, captive-bred

individuals exported for zoos in 2013: three reported by Brazil and one reported by the importer. Prior to

2006 trade comprised three live individuals from an unknown source directly exported for commercial

purposes in 1992 to countries other than the EU-28, as reported by the importer.

There has never been any reported indirect trade in L. lagotricha originating from Brazil to the EU-28.

Colombia: Colombia has submitted annual reports for the years 2006-2014, but has not yet submitted

an annual report for 2015. Colombia has never published an annual export quota for L. lagotricha.

There were no direct exports of L. lagotricha from Colombia to the EU-28 2006-2015. Direct exports of

L. lagotricha from Colombia to countries other than the EU-28 2006-2015 comprised low quantities

COMMON NAMES: Common Woolly Monkey (EN), Lagothriche de Humboldt (FR), Mono Lanudo (ES)

RANGE STATES: Brazil, Colombia, Ecuador, Peru

UNDER REVIEW: Brazil, Colombia, Ecuador, Peru

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Brazil, Colombia, Ecuador and Peru first applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Vulnerable

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(499) of wild-sourced scientific specimens exported in 2012 and 2014, and 61 wild-sourced derivatives

exported in 2013 for commercial purposes. Prior to 2006 there were low quantities of live individuals

exported.

There has never been any reported indirect trade in L. lagotricha originating from Colombia to the EU-

28.

Ecuador: Ecuador has submitted annual reports for the years 2007-2014, but has not yet submitted

annual reports for 2006 or 2015. Ecuador has never published an annual export quota for L. lagotricha.

There have never been direct exports of L. lagotricha from Ecuador to the EU-28. Direct exports of

L. lagotricha from Ecuador to countries other than the EU-28 2006-2015 comprised two live, captive-

bred individuals exported for zoos in 2009, as reported by Ecuador, and very low volumes (283 in total)

of wild-sourced specimens exported for scientific purposes in 2007 and 2008, as reported by Ecuador.

Prior to 2006, trade consisted of low levels of scientific specimens exported 2000-2003.

There has never been any reported indirect trade in L. lagotricha originating from Ecuador to the EU-28.

Peru: Peru has submitted annual reports for the years 2007-2014, but has not yet submitted annual

reports for 2006 or 2015. Peru has never published an annual export quota for L. lagotricha.

Direct exports of L. lagotricha from Peru to the EU-28 2006-2015 comprised 42 wild-sourced scientific

specimens exported in 2007, as reported by Peru. Direct exports of L. lagotricha from Peru to countries

other than the EU-28 2006-2015 comprised low quantities of wild-sourced scientific specimens exported

in 2011 and 2012 (216 as reported by importers and 62 and 0.11l as reported by Peru). Prior to 2006, there

were low quantities of live individuals exported between 1982 and 2001 which included one wild-

sourced individual.

There has never been any reported indirect trade in L. lagotricha originating from Peru to the EU-28.

Conservation status

Lagothrix lagotricha [L. lagothrix lagothrix] is distributed in south-east Colombia, north-east Ecuador,

north-west Brazil and northern Peru within lowland rainforest and montane forests up to altitudes of

3000 m above sea level (Mittermeier et al., 2013).

Mittermeier et al. (2013) noted that females [L. l. lagothrix and L. l. lugens] mature at around six years of

age, at which time they leave their natal group, while males mature at around eight years. The gestation

period was reported to be between 223 and 225 days, with an average birth interval of 36.7 months, and

that L. lagotricha “may live for more than 30 years” (Mittermeier et al., 2013).

L. lagotricha was categorised as Vulnerable by the IUCN due to predicted future population declines as a

result of hunting and continued habitat loss (Palacios et al., 2008).

Palacios et al. (2008) noted that L. lagotricha was considered common but that it occurred at naturally

low densities. Peres (unpublished data in Peres, 1991) noted that L. lagotricha “was often locally extinct

in areas where three or more years of consistent selective hunting had taken place”.

The species was considered vulnerable to hunting (Altherr, 2007; Palacios et al., 2008), which was

reported to be intensive (Mittermeier et al., 2013). In addition, young animals [L. l. lagotricha and

L. l. lugens] were noted to be frequently captured for pets, with females killed in order for infants to be

taken (Mittermeier et al., 2013).

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Brazil: L. lagotricha [L. l. lagotricha] was noted to occur in north-west Brazil, including in the Pico de

Neblina National Park and Juami-Japurá Ecological Reserve (Mittermeier et al., 2013). The species has

also been reported in Lago Unaçúu within central Amazonia [central-western Brazil] (Haugaasen and

Peres, 2009).

The species was reported to have become locally extinct in a number of areas, including along the

extension of a road into Acre [western Brazilian Amazonia] (Peres, 2001), in Lago da Fortuna, Jaraquí

River and Riozinho River [all central Amazonas State] [including subspecies L. l. cana, L. l. lugens, L. l.

lagotricha, and L. l. poeppigii] as a result of subsistence hunting (Peres, 1990; 1991). In areas in central

Amazonas where hunting was not reported to occur, the species was found to be present, including in

Igarapé, lower Urucu River, upper Urucu River and the upper Tefé River (Peres, 1990; 1991). However,

elsewhere the species was found to be at higher population densities at a site where hunting occurred

(Ponta da Castanha, Tefé River) [Amazonas State], compared to a site with no hunting (Aça-Açaituba,

Tefé River) [Amazonas State] (Johns, 1986 in Peres, 1991). Surveys of Jaú National Park [Amazonas State,

north-western Brazil] in the 1990s reportedly failed to find L. lagotricha, but the authors believed that

there was still a possibility that the species occurred in the park (Barnett et al., 2002). However, José de

Sousa and Silva Júnior (pers. comm. in Barnett et al., 2002) suggested it was likely Lagothrix was extinct

in the Jaú region of the lower Negro River.

Altherr (2007) and Peres (1991) noted that in Brazil the genus Lagothrix was hunted due its large body

size. It was considered a preferred species of subsistence hunters (Constantino, 2016) and Peres (2000)

estimated that the low-income rural population of Brazilian Amazonian hunted between 510 057 and

1 250 539 individuals per year.

In 1989, L. lagotricha was included on the list of species threatened with extinction in Brazil (Instituto

Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, 1989) but Alves and Brito (2013)

reported that of the mammal species in Brazil, L. lagotricha was considered a species of low

conservation priority. Mittermeier et al. (2013) noted that indigenous people have the right to hunt

L. lagotricha, including within protected areas.

Colombia: L. lagotricha [L. l. lagotricha] was reported to occur in the lowlands, east of the Cordillera

Oriental [a branch of the Andes which extends south-west to north-east] across the Amazon river plain

between the Uva River and the Amazon River [south-eastern Colombia] (Defler, 2003). Its northernmost

extent was considered to be at least the northern bank of the Guaviare River [central Colombia]

(Hernández-Camacho and Cooper, 1976). Zárate and Stevenson (2014) reported a population in a forest

fragment in Guaviare [southern central Colombia].

The species [L. l. lagotricha] was classified as ‘least concern’ nationally (Defler, 2003).

In the 1970s, the population density was estimated to be 5.5 individuals/km2 on the Peneya River

(Nishimura and Izawa, 1975 in Palacios et al., 2008). Although the species [L. l. lagotricha] was

considered to have widespread and healthy populations (Defler et al., 2003), Mittermeier et al. (2013)

noted that the majority of populations of L. lagotricha [including L. l. lagotricha and L. l. lugens] in

forests alongside rivers, from the foot of the mountains to the flat regions, had been extirpated.

In 1976, L. lagotricha [including all subspecies] was considered to be “probably the most persecuted

primate species in Colombia” (Hernández-Camacho and Cooper, 1976). No information regarding

current levels of hunting of the species were found.

Camacho and Defler (1985), noted that L. lagothricha (including L. l. lugens) was protected in Nevado de

Huila, Puracé, Cueva de los Guacharos and Picachos Natural National Parks and possibly protected in

Chingaza and Pisba Natural National Parks. Its distribution [L. l. lagothricha] reportedly included

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Amacayacu, Cahuinarí, La Paya and Serranía de Chiribiquete National Natural Parks and Nukak

National Reserve (Mittermeier et al., 2013).

Ecuador: L. lagotricha [L. l. lagotricha] was noted to occur in north-eastern Ecuador, east of the Andes

(de la Torre, 2012) at altitudes between 200 and 1400 m above sea level (Tirira, 2007 in Palacios et al.,

2008.

L. lagotricha was included in Ecuador’s national red book of mammals as ‘vulnerable’ in 2001 (de la Torre

2010) and 2011 (Tirira, 2011). No estimates of population size were found.

Sirén et al. (2004; 2006) reported population declines in Sarayaku [eastern Ecuador], due to

overharvesting, and Sirén et al. (2006) noted that L. lagothricha had declined in the area, only

maintaining a strong population in the “remotest corners of the community’s 1000 km2 hunting ground”.

In an area of Napo Province [north-east central Ecuador], the species was considered locally extinct due

to subsistence hunting (Mena et al., 2000).

L. lagotricha was reported to be overexploited by indigenous communities in almost all settlements

surveyed (de la Montaña, 2013). Altherr (2007) noted that at least four indigenous groups were known to

hunt primates, of which L. lagotricha was considered the most sought after. The off-take of subsistence

hunting was considered to be unsustainable in several areas (Sirén et al., 2004; Altherr, 2007).

There was reportedly no national action plan for primates in Ecuador (de la Torre, 2012). The species

was reported to occur within several protected areas, including Sumaco-Napo Galeras National Park,

Cayambe-Coca and Cofán-Bermejo Ecological Reserve and Cuyabeno Wildlife Reserve (Mittermeier et

al., 2013).

Chapter 3, Article 5 of Agreement No. 143 permits indigenous people to hunt wildlife for subsistence

purposes but prohibits the selling of any wildlife products for profit (Ministerio del Ambiente, 2002).

However, enforcement of the law concerning trade of wild animals was reported to be weak (de la Torre,

2012).

Peru: L. lagotricha was reported to occur in the Loreto Region [north-eastern Peru] between the Napo

River and Putumayo River, north of the Amazon River between altitudes of 72 and 219 m above sea level

(MINAM, 2011). Alvard et al. (1997) also report the presence of L. lagotricha in Yomiwato [in Manú

National Park, south-eastern Peru].

The species was noted to have been eradicated in some areas of the Maijuna Regional Conservation Area

before the site was protected (Bravo, 2010 in MINAM, 2011). Bennett et al. (2001) reported only one

sighting of L. lagotricha during line transect surveys of a study area along the Tapiche River between

March and September 1997. MINAM (2011) noted that there was insufficient evidence on L. lagotricha in

Peru to accurately assess the population status, although inferred that the population was in decline due

to the decline of available habitat and exploitation of the species.

The species was considered highly sought after for the pet trade and was noted to be easy to acquire in

the main Amazonian cities (MINAM, 2011). It was also considered threatened by subsistence hunting,

although due to increased ease of transport and availability of weapons, subsistence hunting was noted

to have changed to commercial hunting in some areas, with increased off-take (MINAM, 2011).

Loreto Province, in which the species was reported to occur, includes several protected areas: Majuna-

Kichwa, classified as a regional conservation area in 2015 (Sanborn et al., 2016), Yaguas Reserved Zone

created in 2011 (Frankfurt Zoological Society, 2016), as well as two proposed regional conservation areas:

Algodón Medio Putumayo and Bajo Putumayo-Yagua (MINAM, 2011). MINAM (2011) noted that if the

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Lagothrix lagotricha

proposed regional conservation areas (to include Majuna which has since been classified) were

implemented, it would provide greater protection for L. lagotricha.

The Supreme Decree no. 34-2004-AG prohibits hunting, capturing, owning, transporting and exporting

of threatened species for commercial purposes, which includes L. lagotricha, which was listed as

‘vulnerable’ on the decree (Heymann, 2004; MINAM, 2011). Palomino (pers. comm. 2006 in Altherr,

2007) noted that enforcement of the law was weak and that the meat of L. lagotricha was openly sold.

Ikamaperu, a sanctuary near Moyobamba in the Mayo River Valley, was reportedly rehabilitating and

releasing former pet monkeys, focusing on woolly and spider monkeys (Palomino pers. comm. 2005 in

Altherr, 2007).

References

Altherr, S. 2007. Going to Pot. The neotropical bushmeat crisis and its impact on primate populations. Munich. 27 pp. Alvard, M.S., Robinson, J.G., Redford, K.H., Kaplan, H. and Robinson, G.S. 1997. The sustainability of subsistence

hunting in the neotropics. Conservation Biology, 11(4): 977–982. Alves, D.M.C.C. and Brito, D. 2013. Priority mammals for biodiversity conservation in Brazil. Tropical Conservation

Science, 33(4): 545–550. Barnett, A.A., Borges, S.H., de Castilho, C. V., Neri, F.M. and Shapley, R.L. 2002. Primates of the Jaú National Park,

Amazonas, Brazil. Neotropical Primates, 10(2): 65–70. Bennett, C.L., Leonard, S. and Carter, S. 2001. Abundance, diversity, and patterns of distribution of primates on the

Tapiche River in Amazonian Peru. American Journal of Primatology, 54: 119–126. Bravo, A. 2010. Mamíferos. In: Rapid Inventories Biological and Social. Report 22. The Field Museum, Chicago. 90–96. Camacho, J. and Defler, T. 1985. Some aspects of the conservation of non-human primates in Colombia. Primate

Conservation, 6: 42–50. Constantino, P. 2016. Deforestation and hunting effects on wildlife across Amazonian indigenous lands. Ecology and

Society, 21(2). Defler, T.R. 2003. Primates de Colombia. Conservación Internacional. Bogotá, D.C Defler, T.R., Rodríguez-M, J. V. and Hernández-Camacho, I.J. 2003. Conservation Priorities for Colombian Primates.

Primate Conservation, 19: 10–18. Dew, J.L. 2005. Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha

poeppigii and Ateles belzebuth belzebuth. International Journal of Primatology, 26(5): 1107–1135. Frankfurt Zoological Society 2016. New partnerships for Yaguas Reserved Zone. Available at:

https://peru.fzs.org/en/stories-peru/nuevas-alianzas-para-yaguas/. [Accessed: 2 August 2016]. Groves, C.P. 2001. Primate taxonomy. Smithsonian Institution, Washington D.C. 350 pp. Haugaasen, T. and Peres, C.A. 2009. Interspecific primate associations in Amazonian flooded and unflooded forests.

Primates, 50(3): 239–251. Hernández-Camacho, J. and Cooper, R.W. 1976. The nonhuman primates of Colombia. In: R. W. Thorington, J. and

Heltne, P.G. (Eds.). Neotropical Primates: Field Studies and Conservation. National Academy of Sciences, Washington, DC. 35–69.

Heymann, E.W. 2004. Conservation categories of Peruvian primates- categorias de conservación de los primates Peruanos. Neotropcial Primates, 12(3): 154–155.

Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis 1989. Portaria no 1.522, de 19 de Dezembro de 1989.

Johns, A.D. 1986. Effects of habitat disturbance on rainforest wildlife in Brazilian Amazonia. Unpublished report to World Wildlife Fund-US, Washington, DC.

Mena, P. V, Stallings, J.R., Regalado, J.B. and Cueva, R.L. 2000. The sustainability of current hunting practices by the Huaorani. Robinson, J.G. and Bennett, E.L. (Eds.). Columbia University Press. 57–78 pp.

de la Montaña, E. 2013. Cacería de subsistencia de distintos grupos indígenas de la Amazonía ecuatoriana. Ecosistémas, 22(2): 84–96.

MINAM 2011. Informe Final del Estudio de Especies CITES de Primates Peruanos. Ministerio del Ambiente 2002. Acuerdo No 143 - Normas para el control de la cacería, vedas y licencias de cacería de

especies de fauna silvestre. Government of Ecuador, Ecuador. 2–11 pp. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (Eds.) 2013. Handbook of the mammals of the world. Vol. 3

Primates. Lynx Edicions, Barcelona, Spain. 951 pp. Nishimura, A. and Izawa, K. 1975. The group characteristics of woolly monkeys (Lagothrix lagothricha) in the upper

Amazonian basin. In: Kondo, S., Kaeai, M., Ehara, A. and Kawamura, S. (Eds.). Proceedings from the Symposia of the Fifth Congress of the International Primatological Society. Tokyo, Japan.

Palacios, E., Boubli, J.P., Stevenson, P., Di Fiore, A. and de la Torre, S. 2008. Lagothrix lagotricha. The IUCN Red List

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of Threatened Species 2008. Available at: http://www.iucnredlist.org. [Accessed: 1 August 2016]. Palomino, H. 2006. H. Palomino pers. comm. to PRO WILDLIFE. Palomino, H. 2005. H. Palomino pers. comm. to PRO WILDLIFE. Peres, C. 1991. Humboldt’s woolly monkeys decimated by hunting in Amazonia. Oryx, 25(2): 89–95. Peres, C.A. 1990. Effect of hunting on western Amazonian primate communities. Biological Conservation, 51(1): 47–

59. Peres, C.A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests.

Conservation Biology, 14(1): 240–253. Peres, C.A. 2001. Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest

vertebrates. Conservation Biology, 15(6): 1490–1505. Sanborn, C.A., Hurtado, V. and Ramírez, T. 2016. Consulta previa in Peru: Moving forward. Available at:

http://www.as-coa.org/sites/default/files/2015_CP_PERU_June_17.pdf. [Accessed 1 August 2016]. Sirén, A., Hambäck, P. and Machoa, J. 2004. Including spatial heterogeneity and animal dispersal when evaluating

hunting. Conservation Biology, 18(5): 1315–1329. Sirén, A.H., Cardenas, J.C. and Machoa, J.D. 2006. The relation between income and hunting in tropical forests: an

economic experiment in the eield. Ecological and Society, 11(1). Tirira, D. 2007. Guía de Campo de los Mamíferos del Ecuador. Ediciones Murciélago Blanco, Quito (Ecuador). Tirira, D.G. 2011. Libro rojo de los mamíferos del Ecuador. 2a. edició. Fundación Mamíferos y Conservación, Pontificia

Universidad Católica del Ecuador y Ministerio del Ambiente del Ecuador. Publicación especial sobre los mamíferos del Ecuador 8. Quito. 383-386 pp.

de la Torre, S. 2012. Conservation of Neotropical primates: Ecuador - a case study. International Zoo Yearbook, 46: 25–35.

de la Torre, S. 2010. Los primates ecuatorianos, estudios y perspectivas. Avances en Ciencias e Ingenierías, 2: 27–35. Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed.

The John Hopkins University Press, Baltimore, USA. 2142 pp. Zárate, D.A. and Stevenson, P.E. 2014. Behavioral ecology and inter-individual distance of woolly monkeys

(Lagothrix lagothricha) in a rainforest fragment in Colombia. In: The Woolly Monkey. 227–245.

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Lagothrix lugens

PRIMATES: ATELIDAE

Lagothrix lugens II/B

Taxonomic note

See Lagothrix lagotricha for taxonomic information.

Trade patterns

Lagothrix lugens was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

There has never been any reported trade in L. lugens from Colombia or Venezuela to the EU-28 or

elsewhere. There was also no reported trade from either country in L. lagotricha prior to the elevation of

L. lugens, apart from one skull exported indirectly in 1988 from Venezuela. These countries have also

never produced export quotas for the species.

Conservation status

Colombia: Lagothrix lugens was reported to occur within lowland forest in the upper Amazon basin and

Andean forest in Colombia (Botero et al., 2010) up to altitudes of 3000 m above sea level (Defler, 1996;

Stevenson and Link, 2008).

Within its current distribution, L. lugens [L. l. lugens] was considered more common through the

piedmont forest of the Uribe region [central-western Colombia], between La Macarena and the

Cordillera Oriental and in the Serranía la Macarena (Stevenson and Link, 2008), than north of the

Guayabero River where it was considered scarce (Klein and Klein, 1976). Its range continues north to the

eastern slopes of the Cordillera Oriental, as well as in central Colombia from the upper Magdalena

Valley southwards to at least southern Tolima (Stevenson and Link, 2008). There was also noted to be an

“isolated enclave in the Serranía de San Lucas in south-eastern Bolivar and northern Antioquia” in the

north of the Central Cordillera (Stevenson and Link, 2008). Stevenson and Link (2008) added that the

species historically occurred in the southern part of the department of Cesar but that it was “almost

certainly extinct there today”. Defler (1996) noted that L. lugens [L. l. lugens] had the smallest range of

L. lagotricha, L. cana, L. poeppigii and L. lugens.

SYNONYM: Lagothrix lagotricha lugens

COMMON NAMES: Colombian Woolly Monkey (EN), Mono Barrigudo (ES)

RANGE STATES: Colombia, Bolivarian Republic of Venezuela (distribution uncertain)

UNDER REVIEW: Colombia, Bolivarian Republic of Venezuela

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Colombia and the Bolivarian Republic of Venezuela first applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Critically Endangered

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Mittermeier et al. (2013) reported that L. lagotricha and L. lugens had the same reproductive timings;

Stevenson and Link (2008) considered the late maturity and long inter-birth intervals to hinder the

species’ ability to recover from hunting and other threats.

The IUCN considered the species to be endemic to Colombia and categorised L. lugens as Critically

Endangered, due to predicted future population declines as a result of hunting for food and habitat loss

(Stevenson and Link, 2008). However, the national assessment listed L. lugens [L. l. lugens] as

‘vulnerable’ in Colombia in 2010 (Ministerio de Ambiente Vivienda y Desarrollo Territorial, 2010).

Infants [L. l. lugens] were noted to be frequently captured for pets, with females killed in order for the

young to be taken (Mittermeier et al., 2013). Based on a survey in Tinigua National Park, Lizcano et al.

(2014) calculated that if more than 2 per cent of females within a population are hunted each year, it can

quickly lead to population collapse.

Stevenson et al. (2010) noted that Tinigua National Park [central Colombia] had the highest population

densities of Lagothrix. Stevenson (2007) reported an increase in population density within his study area

near the Macarena mountains in Tinigua National Park from 41 individuals/km2 in 1996 to

50 individuals/km2 in 2000, although Lizcano et al. (2014) noted that the high population density in

Tinigua National Park was uncommon. Defler (1996) estimated the population density in a study area on

the Duda River in Tinigua National Park to be 28 individuals/km2 based on data from Steven et al.

(unpublished 1994). Defler (1996) extrapolated his population density estimate across the forested area

of Tinigua National Park and reported an “optimistic approximate population of 54 404 Lagothrix of

which 27 200 were estimated to be adults”. He added that although a census had not been carried out,

he personally believed the population of mature L. lugens [L. l. lugens] could have been 20 000

individuals in 1996 due to the large area of occupancy (Defler, 1996).

In Cueva de los Guacharos National Park [south-western Colombia], Vargas et al. (2013) carried out line

transect surveys between 2009 and 2010 and estimated the population of L. lugens [L. l. lugens] to be

20.5 individuals/km2.

The species was noted to occur in three contiguous protected areas (Stevenson and Link, 2008): La

Macarena National Park, Tinigua National Natural Park [L. l. lugens] (Defler, 1996; Stevenson et al.,

1994) and Cordillera de los Picachos Natural National Park [L. l. lugens] (Defler, 1996; Defler, 2004) [all

in central Colombia], as well as within Cueva de los Guacharos Natural National Park [south-west

Colombia] (INDERENA, 1989 in Stevenson and Link, 2008; Defler, 1996). The species [L. l. lugens] was

also reported from Alto Fragua Indi-Wasi National Park (Negret et al., 2015), Puracé and El Cocuy

National Parks and considered likely to occur in Chingaza National Park (Defler, 1996).

Bolivarian Republic of Venezuela: In 1976, Hernández-Camacho and Cooper (1976) noted the

presence of a recently discovered population of L. lugens [L. l. lugens] in an area of dense piedmont

forest in the Sarare River drainage, Apure State, near the Colombian border. Defler (1996) referred to

this population as unconfirmed. Bodini and Pérez-Hernández (1987) noted that woolly monkeys had not

been collected in Venezuela, but expected that L. lugens [L. l. lugens] occurred in Selva de San Camilo in

Apure State. No other reports of the occurrence of the species in Venezuela were found.

L. lugens was not listed in the national red lists for fauna in 2015 (Rodríguez et al., 2015) or in 2008

(Rodríguez and Rojas-Suárez, 2008).

References

Bodini, R. and Pérez-Hernández, R. 1987. Distribution of the species and subspecies of cebids in Venezuela. Fieldiana, 39: 231–244.

Botero, S., Rengifo, L.Y., Bueno, M.L. and Stevenson, P.R. 2010. How Many Species of Woolly Monkeys Inhabit

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Colombian Forests? American Journal of Primatology, 72: 1131–1140. Defler, T.R. 2004. Primates of Colombia. Conservation International, Washington DC. - pp. Defler, T.R. 1996. The IUCN conservation status of Lagothrix lagothricha lugens Elliott, 1907. Neoptropical Primates,

4(3): 78–80. Hernández-Camacho, J. and Cooper, R.W. 1976. The nonhuman primates of Colombia. In: R. W. Thorington, J. and

Heltne, P.G. (Eds.). Neotropical Primates: Field Studies and Conservation. National Academy of Sciences, Washington, DC. 35–69.

Instituto Nacional de los Recursos Naturales Renovables y del Medio Ambiente (INDERENA) 1989. A Guide to the National Natural Parks System of Colombia. Bogota, Colombia.

Klein, L.L. and Klein, D.J. 1976. Neotropical primates: Aspects of habitat usage, population density, and regional distribution in La Macarena, Colombia. In: Thorington, J.R.W. and Heltne, P.G. (Eds.). Neotropical Primates: Field Studies and Conservation. National Academy of Sciences, Washington D. C., USA. 70–78.

Lizcano, D.J., Ahumada, J.A., Nishimura, A. and Stevenson, P.R. 2014. Population viability analysis of woolly monkeys in western Amazonia. In: The Woolly Monkey. 267–282. Springer, New York.

Ministerio de Ambiente Vivienda y Desarrollo Territorial 2010. Resolución número 383, 23 de febrero de 2010. República de Colombia. - pp.

Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (Eds.) 2013. Handbook of the mammals of the world. Vol. 3 Primates. Lynx Edicions, Barcelona, Spain. 951 pp.

Negret, P.J., O., G. and Stevenson, P.R. 2015. First preliminary inventory of Non-Flying Mammals of the Alto Fragua Indi-Wasi National. Mammalogy Notes, 1(2): 32–35.

Rodríguez, J.P., García-Rawlins, A. and Rojas-Suárez, F. 2015. Libro rojo de la fauna Venezolana. Available at: http://animalesamenazados.provita.org.ve/. [Accessed: 5 August 2016].

Rodríguez, J.P. and Rojas-Suárez, F. 2008. Libro rojo de la fauna Venezolana. Tercera Ed. Provita y Shell Venezuela, Caracas, Venezuela.

Stevenson, P., Guzman, D.C. and Defler, T.R. 2010. Conservation of Colombian primates : an analysis of published research. Tropical Conservation Science, 3(1): 45–62.

Stevenson, P. and Link, A. 2008. Lagothrix lugens. The IUCN Red List of Threatened Species 2008. Available at: http://www.iucnredlist.org [Accessed: 5 August 2016].

Stevenson, P.R. 2007. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In: Seed dispersal: theory and its application in a changing world. CAB International, New York. 340–362.

Stevenson, P.R., Quinones, M.J. and Ahamuda, J.A. 1994. Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia. American Journal of Primatology, 32(2): 123–140.

Vargas, S.A., León, J., Ramírez, M., Galvis, N., Cifuentes, E. and Stevenson, P.R. 2013. Population Density and Ecological Traits of Highland Woolly Monkeys at Cueva de los Guacharos National Park, Colombia. In: High Altitude Primates. Springer, New York 85–102.

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Lagothrix poeppigii

PRIMATES: ATELIDAE

Lagothrix poeppigii II/B

Taxonomic note

See Lagothrix lagotricha for information on taxonomy.

Trade patterns

Lagothrix poeppigii was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

Brazil: Brazil has submitted annual reports for the years 2006-2014, but has not yet submitted an annual

report for 2015. Brazil has never published an annual export quota for L. poeppigii.

There has never been any reported direct or indirect trade in L. poeppigii from Brazil to the EU-28 or

countries other than the EU-28. Prior to the 2013 elevation of L. poeppigii to species level there were very

low volumes of trade in L. lagotricha from Brazil, which could have included trade in this species (see

L. lagotricha trade patterns section).

Ecuador: Ecuador has submitted annual reports for the years 2007-2014, but has not yet submitted

annual reports for 2006 or 2015. Ecuador has never published an annual export quota for L. poeppigii.

There have never been direct exports of L. poeppigii from Ecuador to EU-28. Direct exports of

L. poeppigii from Ecuador to countries other than the EU-28 2006-2015 comprised two live, captive-bred

individuals exported for zoos in 2009 (reported by Ecuador) and very low volumes of wild-sourced

scientific specimens 2007-2014 (Table 1).

There has never been any reported indirect trade in L. poeppigii originating from Ecuador to the EU-28.

Prior to the 2013 elevation of L. poeppigii to species level there were very low volumes of trade in

L. lagotricha from Ecuador, which could have included trade in this species (see L. lagotricha trade

patterns section).

SYNONYM: Lagothrix lagotricha poeppigii

COMMON NAMES: Poeppig’s Woolly Monkey (EN), Lagotriche de Castelnau (FR), Mono Laudo Pateado (ES)

RANGE STATES: Brazil, Ecuador, Peru

UNDER REVIEW: Brazil, Ecuador, Peru

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Brazil, Ecuador and Peru first applied on 24/09/2000 and last confirmed on 28/05/2015.

IUCN: Vulnerable

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Table 1: Direct exports of Lagothrix poeppigii from Ecuador to the rest of the world (RoW), 2006-2015. No trade was reported 2006, 2011-2012 or 2015.

Importer Term Unit Purpose Source Reported by 2007 2008 2009 2010 2013 2014

RoW live - Z C Importer

Exporter 2

specimens L S I Importer 15

Exporter

- W Importer 4

Exporter 8 33 32 1 3 8

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 03/08/2016.

Peru: Peru has submitted annual reports for the years 2007-2014, but has not yet submitted annual

reports for 2006 or 2015. Peru has never published an annual export quota for L. poeppigii.

Direct exports of L. poeppigii from Peru to EU-28 2006-2015 comprised very small quantities (2.14 kg) of

wild-sourced specimens exported in 2012 and 2014 for scientific purposes, as reported by Peru and

importers. Direct exports of L. poeppigii from Peru to countries other than the EU-28 2006-2015

comprised 0.3 kg of wild-sourced bodies for scientific purposes exported in 2014, as reported by the

importer.

There has never been any reported indirect trade in L. poeppigii originating from Peru to the EU-28.

Prior to the 2013 elevation of L. poeppigii to species level there were low volumes of trade in L. lagotricha

from Peru, which could have included trade in this species (see L. lagotricha trade patterns section).

Conservation status

Lagothrix poeppigii occurs in eastern Ecuador, northern and eastern Peru and in north-west Brazil

(Mittermeier et al., 2013). Mittermeier et al. (2013) noted that the species occurred in primary and some

secondary lowland and high elevation forest, while Stevenson et al. (2008) stated that the species did not

occur in secondary or disturbed forests.

L. poeppigii [L. l. poeppigii] was noted to have a low reproductive rate (Ramirez, 1988 in Calouro, 1999),

with a gestation period of around 225 days (Mittermeier et al., 2013). Females were reported to reach

sexual maturity at around eight years of age (Walder, 2014).

The species was categorised as Vulnerable by the IUCN due to past population declines as a result of

hunting and habitat loss (Stevenson et al., 2008). Stevenson et al. (2008) noted that subsistence and

market hunting for food and habitat loss were the greatest threats to the species, and it was considered

to have a decreasing population trend. Ramirez (1988 in Calouro, 1999) considered L. poeppigii

[L. l. poeppigii] very sensitive to hunting pressure.

Captive populations of L. poeppigii were considered to be in decline (Walder, 2014) and associated with a

range of health issues (Ange-Van Heugten et al., 2008). Due to this, captive breeding programmes were

considered not viable (Ange-Van Heugten et al., 2008).

Brazil: L. poeppigii was reported to occur within the states of Acre and Amazonas, in north-west Brazil

(Stevenson et al., 2008). Ravetta et al. (2014) noted that there had been local extinctions of the species

but did not provide details of where these had occurred.

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The species was listed as ‘vulnerable’ on the Brazilian Endangered species list in 2014, as it was suspected

that the population had declined by at least 30 per cent within three generations (Ravetta et al., 2014). In

an assessment of Brazil’s mammal species, Alves and Brito (2013) listed L. poeppigii as medium priority

for conservation.

Hunting was considered the greatest threat due to increased use of firearms and increased access to

remote areas, particularly in the state of Acre (Ravetta et al., 2014). Altherr (2007) and Peres (1991) noted

that in Brazil the genus Lagothrix was hunted due its large body size.

The species’ occurrence was reported from the protected areas of Serra do Divisor National Park

[L. l. poeppigii] (Calouro, 1999), Jutaí-Solimões Ecological Station, Javarí-Burití Area of Ecological

Interest (Stevenson et al., 2008) and Cujubim Sustainable Development Reserve (unpublished data in

Ravetta et al., 2014).

Ecuador: The species was noted to occur east of the Andes (de la Torre, 2012) south of the Napo and

Amazonas rivers, below altitudes of 1800 m above sea level (Stevenson et al., 2008).

L. poeppigii was included in Ecuador’s national red book of mammals as ‘vulnerable’ in 2011 (Tirira, 2011).

It was reported that in lowland Ecuador the species has not been hunted and was “the most abundant

primate in terms of biomass and number of individuals” (T. de Fiore pers. comm. in Stevenson et al.,

2008).

Several population studies have taken place in Yasuní National Park:

Dew (2005) studied L. poeppigii [L. l. poeppigii] for 18 months and estimated the density to be

around 31 individuals/km2 with home ranges of around 100-120 ha;

Di Fiore (2003) carried out a study between April 1995 and March 1996 and reported home

ranges of three groups of L. poeppigii [L. l. poeppigii] as 124 ha, 108 ha and 105 ha. Di Fiore (2003;

2004) noted that L. poeppigii [L. l. poeppigii] was the most numerous and frequently

encountered of the 10 resident primate species in the 650 ha study area;

Papworth et al. (2013) assessed two sites 26 km apart within Yasuní National Park; Yasuní

Research Station, which was considered to have a higher hunting pressure, and Tiputini

Biodiversity Station which was considered to have a low hunting pressure. They estimated the

population density to be 20.4 individuals/km2 at Yasuní Research Station and 31.89

individuals/km2 at Tiputini Biodiversity Station.

The species was considered threatened by habitat loss and overexploitation (de la Torre, 2012).

Indigenous hunters reportedly target large species including L. poeppigii, and the species was

overexploited by indigenous communities in almost all settlements surveyed (de la Montaña, 2013).

Hunting reportedly also occurred within Yasuní National Park (Di Fiore and Fleischer, 2005; Papworth

et al., 2013). It was estimated that the hunting offtake was 200 individuals a year from an area of 800 km2

at Yasuní Research Station (Papworth et al., 2013 derived from Franzen, 2006). Bass et al. (2010) noted

that hunting of L. poeppigii in Yasuní National Park was unsustainable.

Chapter 3, Article 5 of Agreement No. 143 permits indigenous people to hunt wildlife for subsistence

purposes but prohibits the selling of any wildlife products for profit (Ministerio del Ambiente, 2002). In

2012 there was reportedly no national action plan for primates in Ecuador, and enforcement of the law

concerning trade of wild animals was noted to be weak (de la Torre, 2012).

A non-profit foundation called Sumak Allpa reportedly established a rehabilitation program on Sumak

Island to rehabilitate monkeys taken from their natural habitat, and in 2012, three L. poeppigii

[L. l. poeppigii] were reintroduced (Walder, 2014).

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The species has been recorded in several protected areas including Yasuní National Park, Sangay

National Park and Podocarpus National Park (Stevenson et al., 2008).

Peru: MINAM (2011) reported L. poeppigii to occur in the regions of Loreto [north-eastern Peru],

Amazonas [north-central Peru] and Ucayali [central eastern Peru], between altitudes of 89 m and 1180 m

above sea level.

Several surveys have estimated the population density of L. poeppigii in different areas of Peru:

Aquino et al. (2014) carried out transect surveys of the species in Rio Curaray basin [Loreto

Region] between November and December 2012 and estimated the population density of

L. poeppigii to be 49.6 individuals/km2. They noted that L. poeppigii was the most frequently

observed primate species in the survey (Aquino et al., 2014);

Kolowski and Alonso (2012) carried out surveys in the department of Loreto, near the Ecuador

border and estimated the population density to be 30.64 individuals/km2 which they noted

approached the highest estimated density for the species;

Aquino et al. (2009) estimated 15.4 individual/km2 in the Itaya River basin [Loreto Region]

based on transect surveys;

Aquino et al. (2000 in Aquino et al., 2014) estimated 10 individuals/km2 in the Pucacuro River

basin [Loreto Region];

Within Pacaya Samiria National Reserve [Loreto Region], Aquino et al. (2000 in MINAM, 2011)

estimated a population density of 15.1 individuals/km2 in a frequently hunted area and 24.2

individuals/km2 in an infrequently hunted area;

Puertas and Bodmer (1993) surveyed two areas in Tamshiyacu-Tahuayo Communal Reserve

[Loreto Region] between June 1990 and August 1992. They estimated a density of 7.2

individuals/km2 in the Tahuayo-Blanco region of the reserve which they noted experienced a

persistent hunting pressure and estimated 25.7 individuals/km2 in Yavari Miri region which

experienced some occasional hunting pressure. Puertas and Bodmer, (1993) reported this as

L. lagotricha but MINAM (2011) considered this to refer to L. poeppigii.

The species was noted to be threatened by hunting and habitat loss which have caused the loss of

L. poeppigii near human population centres and from some river basins (Aquino and Encarnación, 1994;

CDC, 2002 in MINAM, 2011). Kolowski and Alonso (2012) noted that L. poeppigii was highly prized by

hunters for its meat. Several reports of hunting pressure have been noted; Bodmer et al. (1999) in

Aquino et al. (2009) suggested that off-take of primates should not exceed 10 per cent in order to be

sustainable, however annual harvest rates of 27.3 per cent in the upper Itaya River basin (Aquino et al.,

2009) and 28 per cent in Quebrada Blanco (Salovaara et al., 2003 in MINAM, 2011) were reported.

Furthermore, Aquino et al. (2000 in MINAM, 2011) reported that L. poeppigii was one of the most hunted

species within Pacaya Samiria National Reserve [north-eastern Peru].The Supreme Decree no. 34-2004-

AG prohibits hunting, capturing, owning, transporting and exporting of threatened species for

commercial purposes, including L. poeppigii, which was listed as ‘near threatened’ in the decree

(Heymann, 2004; MINAM, 2011). Palomino pers. comm. (2006 in Altherr, 2007) noted that enforcement

of the law was weak and the meat of L. poeppigii was openly sold.

MINAM (2011) reported that there was a proposal by the regional government to establish six Regional

Conservation Areas in the Loreto region (Varialles de bajo Morona, Campanquis, Aguas Calientes,

Varialles De Alto Tapiche, Yavari-Mirin, Jeberos), which would help to protect L. poeppigii. Ikamaperu, a

sanctuary near Moyobamba in the Río Mayo Valley was reportedly rehabilitating and releasing former

pet monkeys, focusing on woolly and spider monkeys (Palomino pers. comm. 2005 in Altherr, 2007).

L. poeppigii has been reported in several protected areas: Pacaya-Samiria National Reserve, Tamshiyacu-

Tahuayo Communal Reserve (Stevenson et al., 2008), Pucacuro National Reserve, Alto Nanay-

Pintuyacu-Chambira Regional Conservation Area, Cordillera Escalera Regional Conservation Area, Sierra

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del Divisor National Park, Cordillera Azul National Park, Matsés National Reserve (MINAM, 2011).

INRENA (2006) note the presence of L. lagotricha within Allpahuayo-Mishana National Reserve,

although MINAM (2011) consider this to refer to L. poeppigii.

References

Altherr, S. 2007. Going to pot. The Neotropical bushmeat crisis and its impact on primate populations. Munich. 1-27 pp.

Alves, D.M.C.C. and Brito, D. 2013. Priority mammals for biodiversity conservation in Brazil. Tropical Conservation Science, 33(4): 545–550.

Ange-Van Heugten, K., Timmer, S., Jansen, W.L. and Verstegen, M.W.A. 2008. Nutritional and health status of woolly monkeys. International Journal of Primatology, 29(1): 183–194.

Aquino, R., Bodmer, R.E. and Pezo, E. 2000. Evaluación de primates en la cuenca del río Pucacuro, Amazonía peruana. In: La Primatología en el Perú, Volumen 1. Proyecto Peruano de Primatología, Lima. 92–100.

Aquino, R. and Encarnación, F. 1994. Primates of Peru. Primate Report, 40: 1–127. Aquino, R., López, L., García, G. and Heymann, E.W. 2014. Diversity, abundance and habitats of the primates in the

Río Curaray basin, Peruvian Amazonia. Primate Conservation, (28): 1–8. Aquino, R., Terrones, W., Navarro, R., Terrones, C. and Cornejo, F.M. 2009. Caza y estado de conservación de

primates en la cuenca del río Itaya, Loreto, Perú. Revista Peruana de Biología, 15(2): 33–39. Bass, M.S., Finer, M., Jenkins, C.N., Kreft, H., Cisneros-Heredia, D.F., McCracken, S.F., Pitman, N.C.A., English, P.H.,

Swing, K., Villa, G. et al. 2010. Global conservation significance of Ecuador’s Yasuní National Park. Hector, A. (Ed.). PLoS ONE, 5(1): 22.

Bodmer, R., Allen, C., Penn, J., Aquino, R. and Reyes, C. 1999. Evaluación del uso sostenible de la fauna silvestre en la Reserva Nacional Pacaya Samiria. Documento de trabajo América verde 4b.

Calouro, A.M. 1999. Riqueza de mamíferos de grande e médio porte do Parque Nacional da Serra do Divisor (Acre, Brasil). Revista Brasileira de Zoologia, 16: 195–213.

Centro de Datos para la Conservación 2002. Complejo de humedales del Abanico del Río Pastaza, Loreto-Perú. In: World Wildlife Fund (WWF). Universidad Nacional Agraria La Molina. WWF-CDC UNALM, Lima.

Dew, J.L. 2005. Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. International Journal of Primatology, 26(5): 1107–1135.

Di Fiore, A. 2003. Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National National Park, Ecuador. American Journal of Primatology, 59(2): 47–66.

Di Fiore, A. 2004. Diet and feeding ecology of woolly monkeys in a western Amazonian rain forest. International Journal of Primatology, 25(4): 767–801.

Di Fiore, A. and Fleischer, R.C. 2005. Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. International Journal of Primatology, 26(5): 1137–1173.

Franzen, M. 2006. Evaluating the sustainability of hunting: a comparison of harvest profiles across three Huaorani communities. Environmental Conservation, 33(1): 36–45.

Heymann, E.W. 2004. Conservation categories of Peruvian primates- categorias de conservación de los primates Peruanos. Neotropcial Primates, 12(3): 154–155.

INRENA 2006. Plan Maestro de la Reserva Nacional Allpahuayo Mishana 2006-2010. Iquitos: INRENA. 158 pp.

Kolowski, J.M. and Alonso, A. 2012. Primate Abundance in an Unhunted Region of the Northern Peruvian Amazon and the Influence of Seismic Oil Exploration. International Journal of Primatology, 33: 958–971.

MINAM 2011. Informe Final del Estudio de Especies CITES de Primates Peruanos. Ministerio del Ambiente 2002. Acuerdo No 143 - Normas para el control de la cacería, vedas y licencias de cacería de

especies de fauna silvestre. Government of Ecuador, Ecuador. 2–11 pp. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (Eds.) 2013. Handbook of the mammals of the world. Vol. 3

Primates. Lynx Edicions, Barcelona, Spain. 951 pp. de la Montaña, E. 2013. Cacería de subsistencia de distintos grupos indígenas de la Amazonía ecuatoriana.

Ecosistémas, 22(2): 84–96. Palomino, H. 2005. H. Palomino pers. comm. to PRO WILDLIFE. Palomino, H. 2006. H. Palomino pers. comm. to PRO WILDLIFE.Papworth, S., Milner-Gulland, E.J. and Slocombe, K.

2013. Hunted woolly monkeys (Lagothrix poeppigii) show threat-sensitive responses to Human Presence. PLoS ONE, 8(4).

Peres, C. 1991. Humboldt’s woolly monkeys decimated by hunting in Amazonia. Oryx, 25(2): 89–95. Puertas, P. and Bodmer, R.E. 1993. Conservation of a high diversity primate assemblage. Biodiversity and

Conservation, 2: 586–593. Ramirez, M. 1988. The Wolly Monkeys, Genus Lagothrix. In: Ecology and Behavior of Neotropical Primates. WWF,

Vol. 2, Washington D. C. 539–575. Ravetta, A.L., Muniz, C.C. and Rylands, A.B. 2014. Mamíferos - Lagothrix poeppigii - Macaco barrigudo. Available at:

http://www.icmbio.gov.br/portal/faunabrasileira/lista-de-especies/7192-mamiferos-lagothrix-poeppigii-

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macaco-barrigudo. [Accessed: 9 August 2016]. Salovaara, K., Bodmer, R., Recharte, M. and Reyes, C.F. 2003. Diversity and abundance of mammals. In: Pitman, N.,

Vriesendorp, C. and Moskovits, D. (Eds.). Perú: Yavari. Rapid biological inventories Report 11. The Field Museum, Chicago, Illinois. 156–164.

Stevenson, P., Link, P., Fiore, A. Di, de la Torre, S. and Boubli, J.P. 2008. Lagothrix poeppigii. The IUCN Red List of Threatened Species 2008. Available at: http://www.iucnredlist.org. [Accessed: 9 August 2016].

Tirira, D.G. 2011. Libro rojo de los mamíferos del Ecuador. 2a. edició. Fundación Mamíferos y Conservación, Pontificia Universidad Católica del Ecuador y Ministerio del Ambiente del Ecuador. Publicación especial sobre los mamíferos del Ecuador 8. Quito. 383-386 pp.

de la Torre, S. 2012. Conservation of Neotropical primates: Ecuador - a case study. International Zoo Yearbook, 46: 25–35.

Walder, C. 2014. Rehabilitation Assessment of a Juvenile Woolly Monkey (Lagothrix lagotricha poeppigii) troop on Sumak Allpa Island, Ecuador.

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Lophocebus albigena

PRIMATES: CERCOPITHECIDAE

Lophocebus albigena II/B

SYNONYMS: Cercocebus albigena, Lophocebus ugandae

COMMON NAMES: Grey-cheeked Mangabey (EN), Lophocèbe à Joues Grises (FR), Mangabey de Mejillas Grises (ES)

RANGE STATES: Angola, Burundi, Cameroon, Central African Republic, Congo, Democratic Republic of the Congo, Equatorial Guinea, Gabon, Kenya (distribution uncertain), Nigeria, Rwanda, South Sudan, Uganda, United Republic of Tanzania.

UNDER REVIEW: Nigeria

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

Current no opinion for Cameroon, Equatorial Guinea and Uganda formed on 27/01/1999.

IUCN: Least Concern

Taxonomic note

The CITES Standard Reference (Wilson and Reeder, 2005) accepts two subspecies:

Lophocebus albigena johnstoni and Lophocebus albigena osmani. Groves (2007) considered that

L. a. albigena, L. a. johnstoni, L. a. osmani and L. a. ugandae should be classified as separate species and

some of the recent literature considers these as such (Mittermeier et al., 2013). For the purposes of this

review, the nomenclature accepted by the CITES Standard Reference is followed, but for clarification,

the nomenclature used in the literature is given in square brackets.

Trade patterns

Lophocebus albigena was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

Nigeria has submitted annual reports for the years 2006-2009 and 2012, but has not yet submitted

annual reports for 2010-2011 or 2013-2015. Nigeria has never published an annual export quota for

L. albigena.

There has never been any reported direct or indirect trade in L. albigena from Nigeria to the EU-28 or

elsewhere.

Conservation status

Lophocebus albigena was reported to occur in equatorial Africa (Olupot and Waser, 2013), including

south-east Nigeria, Cameroon, Congo, Gabon, Equatorial Guinea, south-west Central African Republic,

Democratic Republic of Congo, Burundi, Uganda, western Kenya and extreme north-west Tanzania

(Oates et al., 2008). L. a. johnstoni [L. johnstoni] was reported to occur east and south of the Ybangi

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River and north of the Congo River in the Democratic Republic of the Congo, western Rwanda, western

Burundi, in north-west Tanzania and “possibly” in Uganda (Mittermeier et al., 2013). L. a. osmani

[L. osmani] reportedly occurs in south-east Nigeria and west central Cameroon. It was noted that its

distribution needed reassessing (Mittermeier et al., 2013).

The species was noted to occur in low elevation primary and secondary forest (Mittermeier et al., 2013).

Females reportedly reach sexual maturity at three years of ages and males at five to seven, and gestation

takes 184-189 days, with single young born every two to four years (Mittermeier et al., 2013). Their life

span is reportedly up to 32.6 years (Rowe, 1996 in National Primate Research Center, 2013).

L. albigena was categorised as Least Concern by the IUCN, as the species was considered to be relatively

widespread and common, although it was noted that localised declines had occurred and the population

was considered to be decreasing (Oates et al., 2008). Oates et al. (2008) noted that the single assessment

of L. albigena, including subspecies, was provisional and required urgent reassessment, as Groves (2007)

accepted four separate species.

Estimated population densities for the species vary between 18 and 77 individuals/km2 (Oates et al.,

2008). Mittermeier et al. (2013) noted that L. a. osmani [L. osmani] was probably locally extinct in some

areas and that L. a. johnstoni [L. johnstoni] had become scarce in some protected areas following civil

war.

The species was considered to be threatened by deforestation and the bushmeat trade (Oates et al.,

2008; Olupot and Waser, 2013; Mittermeier et al., 2013).

All monkeys, including L. albigena were listed as Class B in the African Convention on the conservation

of nature and natural resources (Mittermeier et al., 2013). Species on class B are considered “totally

protected, but may be hunted, killed, captured or collected under special authorization granted by the

competent country” (Organisation of African Unity, 1968).

Nigeria: L. a. osmani [L. osmani] was noted to occur in south-east Nigeria (Olupot and Waser, 2013),

including in Gashaka-Gumti National Park [within Taraba State and Adamawa State] (Sommer and

Ross, 2010), although its distribution was believed to need reassessing (Mittermeier et al., 2013). No

other subspecies of L. albigena were reported to occur in Nigeria (Mittermeier et al., 2013).

Adanu et al. (2010) reported a sighting of a single L. albigena in 2005 within Taraba state [south-east

Nigeria], where it was previously unknown to occur, close to the River Gamgam and Mayo Sabere.

Subsequent sightings in Kwano Forest, also in Taraba State, have since been reported (K. Arnold et al.

pers. comm. in Adanu et al., 2010).

Grubb et al. (2000 in Montemaggiori et al., 2005) noted that L. albigena was considered very rare. Oates

(2011) also considered it “very rare” in the forests of the Nigeria-Cameroon border and Mittermeier et al.

(2013) noted that L. a. osmani [L. osmani] was “probably now locally extinct” in several areas, including

the Okwango division of the Cross River National Park [south-eastern Nigeria, close to the Cameroon

border].

Gashaka Gumti was reported to be the largest National Park in the country, covering 6731 km2 (Sommer

and Ross, 2010). Sommer and Ross (2010) noted that there were limited resources to manage the

National Park and that poachers have been recorded within the park. A conservation and research

initiative, the Gashaka Primate Project, was reportedly involved with assisting the park in management

(Sommer and Ross, 2010).

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In 2002 and 2003, Fa et al. (2006) surveyed bushmeat markets and villages in an area from the right bank

of the Cross River in south-eastern Nigeria along the coast to Cameroon, but L. albigena was not

recorded in any markets or source villages in Nigeria.

Nigeria is a party to the African Convention on the Conservation of nature and natural resources, which

requires contracting states to adopt legislation to prohibit any method of hunting “liable to cause mass

destruction of wild animals” (Organisation of African Unity, 1968). All species of Lophocebus were

included in the first schedule of the Endangered species (control of international trade and traffic) Act

1985, which prohibits their hunting, capture or trade (Government of Nigeria, 1985).

References

Adanu, J., Sommer, V. and Fowler, A. 2010. Hunters, fire, cattle: conservation challenges in eastern Nigeria, with special reference to chimpanzees. In: Sommer, V. and Ross, C. (Eds.). Primates of Gashaka. Springer, New York, Dordrecht, Heidelberg, London. 55–100.

Fa, J.E., Seymour, S., Dupain, J., Amin, R., Albrechtsen, L. and Macdonald, D. 2006. Getting to grips with the magnitude of exploitation: Bushmeat in the Cross–Sanaga rivers region, Nigeria and Cameroon. Biological Conservation, 129(4): 497–510.

Government of Nigeria 1985. Endangered Species (Control of International Trade and Traffic) Act (1985 No. 11). Groves, C.P. 2007. The Endemic Uganda Mangabey, Lophocebus ugandae, and other members of the Albigena-group

(Lophocebus). Primate Conservation, 22(1): 123–128. Grubb P., Oates J.F., White L.J.T., Tooze Z. 2000. Monkeys recently added to the Nigerian faunal list. The Nigerian

Field, 65: 149-158. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (Eds.) 2013. Handbook of the mammals of the world. Vol. 3

Primates. Lynx Edicions, Barcelona, Spain. 951 pp. Montemaggiori, A., Capula, M., Gippoliti, S., Marsden, S.J., Mertens, A., Rondinini, C., Salerno, G. and Sorace, A.

2005. A study of species which are subject to import suspensions according to the article 4.6 of Regulation 338/97. Istituto Ecologia Applicata. 81 pp.

National Primate Research Center, U. of W. 2013. The Life Spans of Nonhuman Primates. Available at: http://pin.primate.wisc.edu/aboutp/phys/lifespan.html. [Accessed: 29 July 2016].

Oates, J.F. 2011. Primates of West Africa. A field guide and natural history. Mittermeir, R.A. and Rylands, A.B. (Eds.). Conservation International, Washington D.C.

Oates, J.F., Groves, C.P. and Ehardt, C. 2008. Lophocebus albigena. The IUCN Red List of Threatened Species 2008. Available at: http://www.iucnredlist.org. [Accessed: 21 July 2016].

Olupot, W. and Waser, P.M. 2013. Lopocebus albigena (also L. osmani, L. johnstoni, L. ugandae). In: Butynski, T., Kingdon, J. and Kalina, J. (Eds.). Mammals of Africa, Volumes II: Primates. Bloomsbury Publishing, London, New Delhi, New York, Sydney. 204–211.

Organisation of African Unity 1968. African convention on the conservation of nature and natural resources. Organisation of African Unity, Algiers.

Rowe, N. 1996. The Pictorial Guide to Living Primates. Pogonias Press, East Hampton, New York. Sommer, V. and Ross, C. 2010. Exploring and protecting West Africa’s primates: The Gashaka Primate project in

context. In: Sommer, V. and Ross, C. (Eds.). Primates of Gashaka. Springer, New York, Dordrecht, Heidelberg, London. 1–38.

Wilson, D.E. and Reeder, D.M. 2005. Mammal species of the world - a taxonomic and geographic reference. 3rd Ed. The John Hopkins University Press, Baltimore, USA. 2142 pp.

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Piliocolobus badius

PRIMATES: CERCOPITHECIDAE

Piliocolobus badius II/B

Taxonomic Note

The taxonomy of Piliocolobus badius has been subject to debate in the literature (Cardini and Elton,

2009; Oates and Ting, 2015). The current CITES Standard Reference (Wilson and Reeder, 2005)

recognises three subspecies (P. b. badius, P. b. temminckii, and P. b. waldronae), whereas some other

recent sources recognise these as distinct species (Mittermeier et al., 2013; Galat-Luong et al., 2016; Oates

et al., 2016a;b). For the purposes of this review, the nomenclature accepted by the CITES Standard

Reference is followed, but for clarification, the nomenclature used in the literature is given in square

brackets.

The recent taxonomic arrangement of the Colobus monkeys either divides the red and olive Colobus

into two genera, Piliocolobus and Procolobus, respectively, or they are considered to belong to

Procolobus with two subgenera, Piliocolobus and Procolobus, for red and olive Colobus respectively

(Mittermeier et al., 2013; Galat-Luong et al., 2016; Oates et al., 2016a;b).

Trade patterns

Piliocolobus badius was listed in Appendix II on 04/02/1977 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Primates.

There has never been any reported trade in P. badius from Gambia, Ghana, Senegal or Sierra Leone to

the EU-28 or elsewhere. These countries have also never produced export quotas for the species.

Côte d’Ivoire: Côte d’Ivoire has submitted annual reports for the years 2007-2009 and 2011- 2015, but

has not yet submitted annual reports for 2006 and 2010. Côte d’Ivoire has never published an annual

export quota for P. badius.

Direct exports of P. badius from Côte d’Ivoire to EU-28 2006-2015 comprised very low quantities of wild-

sourced scientific specimens, bone pieces and teeth exported in 2006-2007 and 2014-2015 for scientific

SYNONYMS: Colobus badius, Procolobus badius

COMMON NAMES: Western Red Colobus (EN), Colobe Ferrugineux (FR), Colobo Herrumbroso Occidental (ES)

RANGE STATES: Côte d'Ivoire, Gambia, Ghana, Guinea, Guinea Bissau, Liberia, Senegal, Sierra Leone

UNDER REVIEW: Côte d'Ivoire, Gambia, Ghana, Guinea Bissau, Liberia, Senegal, Sierra Leone

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Côte d'Ivoire, Gambia, Ghana, Guinea, Guinea Bissau, Liberia and Senegal and Sierra Leone applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Endangered

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purposes (Table 1). Direct exports of P. badius from Côte d’Ivoire to countries other than the EU-28

2006-2015 comprised two wild-sourced skeletons exported for scientific purposes in 2012.

There has never been any reported indirect trade in P. badius from Côte d’Ivoire to the EU-28.

Table 1: Direct exports of Piliocolobus badius from Côte d’Ivoire to the EU-28 (EU), 2006-2015. All trade was wild-sourced for scientific purposes. No trade was reported 2008-2013 .

Importer Term Unit Reported by 2006 2007 2014 2015

EU bone pieces - Importer 4

Exporter 4

specimens - Importer 3 73 4 120

Exporter 77 4

teeth - Importer 2

Exporter 2

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 03/08/2016

Guinea Bissau: Guinea Bissau has submitted annual reports for the years 2006-2007 and 2009-2014, but

has not yet submitted annual reports for 2008 or 2015. Guinea Bissau has never published an annual

export quota for P. badius.

Direct exports of P. badius from Guinea Bissau to EU-28 2006-2015 comprised seven wild-sourced

scientific specimens exported in 2010, as reported by importers and 12 scientific specimens of unknown

source exported in 2009, as reported by Guinea Bissau. There have never been direct exports of P. badius

from Guinea Bissau to countries other than the EU-28.

There has never been any reported indirect trade in P. badius originating from Guinea Bissau to the EU-

28.

Liberia: Liberia has submitted annual reports for the years 2006-2007 and 2009-2014, but has not yet

submitted annual reports for 2008 or 2015. Liberia has never published an annual export quota for

P. badius.

Direct exports of P. badius from Liberia to EU-28 2006-2015 comprised wild-sourced specimens (46 as

reported by importers) and hairs (46 as reported by Liberia) exported in 2011 for scientific purposes and

one wild-sourced scientific specimen exported in 2014, as reported by importers. There have never been

direct exports of P. badius from Liberia to countries other than the EU-28.

There has never been any reported indirect trade in P. badius originating from Liberia to the EU-28.

Conservation status

Piliocolobus badius is a large monkey endemic to West Africa (Butynski et al., 2013). The species was

reported to range from south-west Senegal and Gambia south-eastwards to south-west Ghana (Butynski

et al., 2013). The subspecies’ occurrence were reported as follows:

Piliocolobus badius badius [P. badius] was reported to occur in Sierra Leone, south Guinea,

Liberia and east to the Nzi-Bandama River system in Côte d’Ivoire (Mittermeier et al., 2013;

Oates et al., 2016a);

Piliocolobus badius temminckii [P. temminckii] was reported to range from the Gambia and

Upper Senegal rivers through south-west Senegal, Gambia, and Guinea Bissau to north-west

Guinea, and possibly occurring in north-west Sierra Leone (Mittermeier et al., 2013), although

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the record from Sierra Leone was considered dubious (N. Ting pers. comm. to Galat-Luong et

al., 2016). Reports of the subspecies from the Fouta Djallon Highlands in Guinea were also

noted, but it was cautioned that there were no published records available to confirm this

(Mittermeier et al., 2013; Galat-Luong et al., 2016);

P. b. waldronae [P. waldronae] was reported to occur in south-east Côte d'Ivoire, and possibly

south-west Ghana (Mittermeier et al., 2013). It previously ranged from the Nzi-Bandama River

system in Côte d’Ivoire to south-western Ghana, but had been extirpated from most of its range

(Mittermeier et al., 2013) and is considered possibly extinct (Oates et al., 2000).

P. b. badius [P. badius] and P. b. temminckii [P. temminckii] were thought to be geographically separated,

although the exact boundary between them was considered to be unclear, while the ranges of

P. b. badius [P. badius] and P. b. waldronae [P. waldronae] were reported to meet at the Bandama River,

Côte d'Ivoire (Mittermeier et al., 2013).

P. b. badius and P. b. waldronae were reported to inhabit primary, moist lowland forest, while

P. b. temminckii was reported to inhabit a variety of forest types including moist lowland forests

(Butynski et al., 2013), as well as dry deciduous and gallery forest, generally near open bodies of water

[P. temminckii] (Mittermeier et al., 2013). P. b. badius and P. b. waldronae were reported to be

particularly sensitive to habitat degradation and fragmentation (Butynski et al., 2013), while

P. b. temminckii [P. temminckii] can adapt to reduced or degraded habitat by becoming increasingly

terrestrial (Galat-Luong and Galat, 2005; Mittermeier et al., 2013). Minhós et al. (2016) suggested that

female P. b. temminckii may be more susceptible to forest disturbance, which restricts their dispersal.

The gestation period was noted to be 198 days, with an interbirth interval of approximately 24 months

(Mittermeier et al., 2013).

P. b. badius [P. badius] and P. b. temminckii [P. temminckii] were categorised as Endangered by the

IUCN, on the basis of estimated population declines of more than 50 per cent over three generations,

principally due to habitat loss and hunting (Oates et al., 2016a; Galat-Luong et al., 2016). Due to the

absence of well-managed protected areas, it was considered that this decline was likely to continue for

P. b. temminckii [P. temminckii], particularly in the southern part of its range where civil war has

persisted and hunting pressure was noted to be increasing (Mittermeier et al., 2013). P. b. waldronae

[P. waldronae] was categorised as Critically Endangered by the IUCN, on the basis of an estimated

population decline of more than 80 per cent over the last three generations, principally due to habitat

loss and hunting (Oates et al., 2016b).

There are no overall population estimates for P. b. badius [P. badius] or P. b. temminckii [P. temminckii],

but the subspecies were noted to be declining across the majority of their range (Oates et al., 2016a;

Galat-Luong et al., 2016). According to Butynski et al. (2013), details of the population size and the extent

of decline were lacking for most sites for all three subspecies, but surviving populations were reported to

be “widely scattered and isolated”. P. b. waldronae [P. waldronae] has not been observed alive in the wild

for over 25 years (Oates et al., 2016b) and was considered probably extinct, although unconfirmed

reports suggest it may still persist in the Tanoé Forest (Côte d’Ivoire) (Mittermeier et al., 2013).

P. badius was reported to be extremely vulnerable to hunting due to its large body size and conspicuous

nature (Butynski et al., 2013). The main threats to P. b. badius [P. badius] were reported to be habitat loss

and hunting (Mittermeier et al., 2013). Subsistence and commercial hunting were reported to have had a

severe impact on populations of P. b. badius [P. badius] and logging roads were reported to have

improved access to remote forest areas resulting in increased hunting (Mittermeier et al., 2013; Oates et

al., 2016a). Habitat loss due to forest conversion was reported to be the main threat to P. b. temminckii

[P. temminckii], coupled with decreased rainfall (Mittermeier et al., 2013). Hunting was also reported to

pose a threat to P. b. temminckii, particularly in the southern part of its range, although it was reported

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to be less affected by this threat than P. b. badius [P. badius] and P. b. waldronae [P. waldronae]

(Mittermeier et al., 2013). Habitat loss and hunting pressure (both subsistence and commercial hunting)

were reported to have been responsible for a massive decline in P. b. waldronae [P. waldronae]

(Mittermeier et al., 2013; Oates et al., 2016b). All three subspecies were reported to have been impacted

by civil war across parts of its range since 1989, although it was considered unclear as to what extent

(Galat-Luong et al., 2016; Oates et al., 2016b).

P. b. badius [P. badius], P. b. temminckii [P. temminckii] and P. b. waldronae [P. waldronae] were all

reported to be listed as Class B in the African Convention on the Conservation of Nature and Natural

Resources (Mittermeier et al., 2013). Species on Class B are considered “totally protected, but may be

hunted, killed, captured or collected under special authorization granted by the competent country”

(Organisation of African Unity, 1968).

In 2005, Montemaggiori et al. (2005) recommended that the restriction on imports for P. badius be

maintained on the basis that the species suffers high levels of hunting and deforestation in range

countries, and that some subspecies were on the verge of extinction. Furthermore, it was reported that

the species suffers high mortality in captivity and no viable captive population existed in zoos worldwide

(Montemaggiori et al., 2005).

Côte d'Ivoire: P. b. badius [P. badius] and P. b. waldronae [P. waldronae] were reported to occur in Côte

d'Ivoire (Oates et al., 2016a; 2016b), although P. b. waldronae was considered possibly extinct (Oates et

al., 2000).

P. b. badius [P. badius] was reported to occur in Taï Forest National Park (Gonedelé Bi et al., 2012;

Mittermeier et al., 2013; Oates et al., 2016a), which was considered to represent the last stronghold of the

subspecies in Côte d’Ivoire (Struhsaker, 2005), containing the only viable population in the country

(Gonedelé Bi et al., 2012). However, high-levels of poaching within the park were reported (Refisch and

Koné, 2005; Struhsaker, 2005).

The population size of P. b. badius was reported to have been reduced by 65 per cent over the previous

10 years and their extent of occurrence and area of occupancy had declined (Gonedelé Bi et al., 2012).

Gonedelé Bi et al. (2012) considered P. p. badius to be ‘endangered’ in the country. P. b. badius was

reported to have been extirpated, mainly due to hunting, from three forest reserves and Marahoué

National Park between the Sassandra and Bandama rivers (Sery et al., 2006) and it was not recorded in

three community forests where it was expected to occur in the south between 2000 and 2008 (Gonedelé

Bi et al., 2012).

It was reported that there have been no confirmed sightings of P. p. waldronae [P. p. waldronae and

P. waldronae] since 1978 and surveys carried out since 1993 had not confirmed the survival of any

individuals (Butynski et al., 2013; Mittermeier et al., 2013). In 2000, Oates et al. (2000) concluded that the

subspecies was probably extinct. Since then, unconfirmed reports, and indirect evidence in the form of a

tail, skin and photograph (McGraw, 2005), from extreme south-eastern Côte d'Ivoire, near Ehy Lagoon

in Tanoé Forest [also referred to as Ehy Forest in the literature], have been noted (Gonedelé Bi et al.,

2008; Mittermeier et al., 2013; Oates et al., 2016b). Tanoé Forest was considered the only place where a

small population of P. b. waldronae may survive (Butynski et al., 2013). P. p. waldronae was considered

‘critically endangered’ in the country and absent in all four forests where it once occurred (Gonedelé Bi

et al., 2012). Furthermore, Gonedelé Bi (2013) did not observe any P. b. waldronae in field surveys of

Tanoé Forest in 2008-2009, which led the authors to conclude that the subspecies was probably extinct

as a result of hunting pressure. It was noted that further surveys of Tanoé Forest were urgently needed

(Butynski et al., 2013; Mittermeier et al., 2013; Oates et al., 2016b).

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Threats to primate species in Côte d'Ivoire were reported to include intensive habitat degradation and

large-scale poaching (Gonedelé Bi et al., 2012). According to Bene et al. (2012), species within protected

areas were also under threat from intensive illegal hunting and “inappropriate conservation measures”.

These threats were reported to be further exacerbated by political and social instability in the country

(Gonedelé Bi et al., 2012).

It was reported that Tanoé Forest was not legally protected, however, in 2006, a pilot community-based

management program for the forest was launched (Gonedelé Bi, 2013) and in 2015, it was reported that

funds were being raised for demarcation to officially designate the forest as a community-managed

forest (Koné et al., 2015).

P. b. badius was listed in Annex I (fully protected) of Law no. 94-442 (amending Law 65-255) on the

protection of wildlife, which prohibits the capture or hunting of the species, except to permit holders

(Côte d’Ivoire, 1994). Hunting and trade of bushmeat and other hunting products was reported to have

been prohibited since 1974, but a lack of control or application of legislation was reported to have

resulted in an increase in wildlife use and trade (Gonedelé Bi et al., 2012).

Gambia: P. b. temminckii [P. temminckii] was reported to occur in Gambia (Galat-Luong et al., 2016).

Populations in Abuko and Pirang [both in western Gambia] were reported to be fragmented (Galat et al.,

2009). Starin (pers. comm. to Galat et al., 2009), highlighted the lack of census data, as well as rapid loss

of known groups of P. b. temminckii and suitable habitat.

In 1989, monkeys in Gambia were reported to be threatened by destruction of habitat, hunting as

agricultural pests, and illegal capture (Starin, 1989). P. b. temminckii [P. temminckii] was reported to be

hunted more as farm pests than for consumption of its meat in Gambia (Mittermeier et al., 2013).

Important sites for the survival of P. b. temminckii in Gambia were reported to include Kiang West

National Park, Bama Kuno Forest Park, Abuko Nature Reserve, Bijilo Forest Park, Pirang Forest Park [all

in western Gambia], River Gambia National Park [central Gambia] and Katilenge Forest Park [south-

western Gambia] (Butynski et al., 2013). The Wildlife Conservation Act, 1977, declared all animals found

in Gambia to be protected (The Republic of Gambia, 1977). The act does not permit hunting or taking of

P. badius (The Republic of Gambia, 1977; de Klemm and Lausche, 1986).

Ghana: P. b. waldronae was previously known only from the western high forests (Oates, 1996) but was

considered possibly regionally extinct in Ghana (Oates et al., 2016b). Surveys carried out since 1993 have

not confirmed the survival of any individuals (Mittermeier et al., 2013). Loss of habitat and hunting of

forest wildlife was reported to have been intense within the range of this subspecies (Oates, 1996).

P. badius was listed under the First Schedule (completely protected) of the Wildlife Conservation

Regulation, 1971, which prohibits the hunting, capture or killing of the species (Ghana, 1971).

Guinea Bissau: P. b. temminckii was reported to previously have been widely distributed in the country

(Galat-Luong and Galat, 2005). The subspecies was reported to occur in southern Guinea-Bissau

(Gippoliti and Dell’Omo, 1996; Galat-Luong and Galat, 2005) and its presence has been reported from

the Cacine basin (Galat-Luong and Galat, 2005) and Cantanhez Forest in the south-west (Gippoliti and

Dell’Omo, 1996), however, the south-eastern limits of its distribution were considered unknown (Galat-

Luong and Galat, 2005). Local accounts of the subspecies’ presence in relict forest patches in the north

(between São Domingos and Susana) have also been noted (Galat-Luong and Galat, 2005).

The subspecies was thought to be rapidly declining (IBAP, 2007) and census data reportedly indicated

the subspecies was disappearing from most areas (Casanova and Sousa, 2007 in Minhós et al., 2016). The

subspecies was reported to occur at high densities in some forests in Cantanhez [south-western Guinea

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Bissau], suggesting that long term conservation is possible, as long as forest patches of certain size and

free of hunting pressure remain (IBAP, 2007). However, Minhós et al. (2016) reported that

P. b. temminckii showed signs of a recent severe demographic collapse, with very low numbers

remaining in Cantanhez National Park (effective population size was estimated below 500 individuals).

The subspecies was reported to be threatened by deforestation and hunting (IBAP, 2007). Cantanhez

National Park was reported to represent one of the last areas retaining tropical forest (Minhós et al.,

2016). However, the forest was reported to be severely fragmented and being lost at a rapid rate, and the

subspecies was reported to be hunted within the park for meat consumption and trade (Costa et al.,

2013; Minhós et al., 2016).

Important sites for the survival of P. b. temminckii in Guinea Bissau were noted to include the Basin of

the Tombali, Cumbija and Cacine Rivers, including the Cantanhez Forest [all in the south-western

Guinea Bissau] (Butynski et al., 2013). P. b. temminckii [P. temminckii] was reported to occur in Cufada

National Park [south-western Guinea Bissau] (Mittermeier et al., 2013; Galat-Luong et al., 2016).

Liberia: Surveys in 1988-1989 found P. p. badius to be common in Liberia (Oates, 1996). In 2005, a rapid

assessment of three Liberian National Parks (North Lorma National Forest [north central Liberia], Gola

National Forest [north-western Liberia] and Grebo National Forest [south-eastern Liberia]) was

undertaken by Barrie et al. (2007). P. p. badius [P. badius] was observed in North Lorma (three

individuals), and Grebo National Forests (25+) (Barrie et al., 2007). The subspecies’ [Procolobus badius]

presence was also reported from Nimba [north-central Liberia] (Galat-Luong and Galat, 2000).

The subspecies [Procolobus badius] was reported to be under threat from increasing human pressure in

Nimba [north-central Liberia] (Galat-Luong and Galat, 2000). Wildlife in Liberia, particularly rare and

threatened mammals, were reported to be threatened by high hunting rates and plans for large-scale

exploitation of natural resources (Tweh et al., 2014). Oates (1996) noted that hunting of primates for

food has been intense. In 2009/1o, a survey of a bushmeat market located on the Liberia – Côte d’Ivoire

border (which received meat daily from the Konobo District of eastern Liberia) observed P. p. badius

[P. badius] (accounting for 9.5 per cent of primates observed) (Covey and McGraw, 2014). The authors

suggested that the rate at which primates are likely being hunted in Liberia’s Konobo District was

approaching unsustainable levels and that without formal protection, could result in the extirpation of

P. p. badius [P. badius], and other vulnerable taxa, in this region in the near future (Covey and McGraw,

2014).

Important sites for the survival of P. b. badius in Liberia were reported to include Grebo National Forest,

Sapo National Park [southern Liberia] and North Lorma National Forest (Butynski et al., 2013). Section

20 of the Liberian Wildlife and National Parks Act, 1988, prohibits hunting in national parks and nature

reserves (Government of Liberia, 1988).

P. b. badius was reported to be fully protected (under Section 60) in the Wildlife and National Parks Act

of 1988 (Government of Liberia, 1988; Forestry Development Authority, 2000).

Senegal: P. b. temminckii [P. temminckii] was reported to occur in south-west Senegal (Galat-Luong et

al., 2016). Extensive surveys of P. b. temminckii carried out in southern Senegal in 1975-1976 and 1988-

2002 concluded that the subspecies was no longer present east of Niokolo Koba National Park [south-

east] and from the area between the park, Gambia and the Casamance [region of Senegal south of

Gambia] (Galat et al., 2009). The population in Niokolo Koba was reported to be separated from those of

Casamance, Saloum [western Senegal] and Guinea (Galat et al., 2009). The northern boundary of the

subspecies’ range was thought to have retreated and its distribution was reported to be “considerably

fragmented”, with the northernmost groups in Saloum reported to be widely separated from each other

(Galat et al., 2009).

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It was reported that there were probably fewer than 100 individuals in Niokolo-Koba National Park and

north-western Guinea (Mittermeier et al., 2013). In the north-western part of its range, the only viable

population was reported from Fathala Forest [in Saloum] (Galat et al., 2009), with an estimated 500

individuals reported by Galat-Luong and Galat (2005).

Significant forest loss and degradation of habitats as a result of major rainfall reductions and human

activities were reported in Fathala Forest, although P. b. temminckii was reported to have adapted to dry

forests and open habitats in Senegal (Galat-Luong and Galat, 2005).

Important sites for the survival of P. b. temminckii in Senegal were reported to include Niokolo-Koba

National Park, Fathala Forest in Saloum Delta National Park, Foret Classee de Patako, Foret Classee de

Sangako and Basse Casamance National Park (Butynski et al., 2013). However, this subspecies may have

been extirpated from Basse Casamance National Park [south-western Senegal] (Mittermeier et al., 2013;

Galat-Luong et al., 2016).

The subspecies is protected under Decree 36 of the Code of Hunting and Wildlife Protection (Senegal,

1986). This decree prohibits the hunting and capture of the species (Senegal, 1986).

Sierra Leone: P. b. badius [P. badius] was reported to occur as fragmented populations (Oates et al.,

2016a) in the high forests of Sierra Leone (Gippoliti and Dell’Omo, 2003). The possible occurrence of

P. b. temminckii [P. temminckii] in north-west Sierra Leone has also been reported (Mittermeier et al.,

2013), however Grubb et al. (1998 in Gippoliti and Dell’Omo, 2003) reported only P. b. badius in the

country and the record of P. b. temminckii [P. temminckii] from Sierra Leone was considered dubious

(N. Ting pers. comm. to Galat-Luong et al., 2016).

Important sites for the survival of P. b. badius in Sierra Leone were reported to include Gola Forest,

Loma Mountains Non-hunting Forest Reserve (under consideration for national park status) and Tiwai

Island (Butynski et al., 2013). P. b. badius [P. badius] was also reported to occur in Outamba-Kilimi

National Park [south-eastern Sierra Leone] (Mittermeier et al., 2013; Oates et al., 2016a).

The Wildlife Conservation Act, 1972, prohibits hunting of any wild animal in national parks, strict

natural reserve or game reserve unless authorised to do so (Government of Sierra Leone, 1972).

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Bene, J.C.K., Kone, I., Gonedele, B.I., Bitty, E.A., Ouattara, K., Akpatou, K.B., N’Guessan, K.A. and Koffi, D.A. 2012. The diurnal primate community of the Tanoé Forest: species composition, relative abundance, distribution, polyspecific associations and conservation status. International Journal of Biological and Chemical Sciences, 6(1): 51–64.

Butynski, T.M., Kingdon, J. and Kalina, J. (Eds.) 2013. Mammals of Africa: Vol. II Primates. Bloomsbury Publishing, London, UK. 560 pp.

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Casanova, C. and Sousa, C. 2007. Action Plan for the Conservation of Chimpanzees, Red Western Colobus and King Colobus in Guinea-Bissau Republic. Guinea-Bissau.

Costa, S., Casanova, C., Sousa, C. and Lee, P. 2013. The good, the bad and the ugly: Perceptions of wildlife in Tombali (Guinea-Bissau, West Africa). Journal of Primatology, 2(1): 1–7.

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Galat, G., Galat-Luong, A. and Nizinski, G. 2009. Increasing dryness and regression of the geographical range of

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Temminck’s red colobus Procolobus badius temminckii: implications for its conservation. Mammalia, 73(4): 365–368.

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Galat-Luong, A. and Galat, G. 2000. Les primates des monts Nimba. Senegal. 21 pp. Galat-Luong, A., Galat, G., Oates, J.F., Struhsaker, T., McGraw, S. and Ting, N. 2016. Piliocolobus temminckii. The

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chimpanzees Pan troglodytes verus and other large mammals in Liberia: a nationwide survey. Oryx, 49(4): 710–718.

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Gyps bengalensis

FALCONIFORMES: ACCIPITRIDAE

Gyps bengalensis II/B

Trade patterns

Gyps bengalensis was listed in Appendix II on 28/06/1979 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Falconiformes.

There has never been any reported trade in G. bengalensis from Bangladesh, Bhutan,

Brunei Darussalam, China, Iran, Lao PDR, Malaysia, Myanmar, the Russian Federation, Thailand or

Viet Nam, to the EU-28 or elsewhere.

Cambodia: Cambodia has submitted annual reports for the years 2006-2014, but has not yet submitted

an annual report for 2015. Cambodia has never published an annual export quota for G. bengalensis.

There have never been any reported direct exports of G. bengalensis from Cambodia to the EU-28.

Direct exports of G. bengalensis from Cambodia to countries other than the EU-28 comprised low

quantities of wild-sourced feathers and scientific specimens exported 2008-2012 (Table 1).

There has never been any reported indirect trade in G. bengalensis originating from Cambodia to the

EU-28.

SYNONYM: Vultur bengalensis

COMMON NAMES: White-rumped Vulture (EN), Vautour Chaugoun (FR), Buitre Leonado Bengalés (ES)

RANGE STATES:

Afghanistan, Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China, India, Islamic Republic of Iran, Lao People’s Democratic Republic, Malaysia, Myanmar, Nepal, Pakistan, Russian Federation, Thailand, Viet Nam

UNDER REVIEW: Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China, Iran, Lao PDR, Malaysia, Myanmar, Nepal, Pakistan, Russian Federation, Thailand, Viet Nam

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Afghanistan, Bangladesh, Bhutan, Brunei Darussalam, Cambodia, China, India, Islamic Republic of Iran, Lao PDR, Malaysia, Myanmar, Nepal, Pakistan, Russian Federation, Thailand, Viet Nam first applied on 29/10/2001 and last confirmed on 28/05/2015. Previous negative opinions for all range states, applied on 07/11/2000.

IUCN: Critically Endangered

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Table 1: Direct exports of Gyps bengalensis from Cambodia to the rest of the world (RoW), 2006-2015. No trade was reported 2006-2007 or 2013-2015. All trade was wild-sourced for scientific purposes.

Importer Term Unit Reported by 2008 2009 2010 2011 2012

RoW feathers - Importer 1318 2083

Exporter 1387 2083

specimens - Importer 210 1216

Exporter 8 210

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 03/08/2016.

Nepal: Nepal has submitted annual reports for the years 2006-2014, but has not yet submitted an

annual report for 2015. Nepal has never published an annual export quota for G. bengalensis.

There was no reported direct or indirect trade in G. bengalensis from Nepal to the EU-28 or countries

other than the EU-28 2006-2015. Prior to 2006 trade comprised very low quantities of wild-sourced

scientific specimens directly exported from Nepal to countries other than the EU-28, as reported by

Nepal.

Pakistan: Pakistan has submitted all annual reports for the years 2006-2015. Pakistan has never

published an annual export quota for G. bengalensis.

Direct exports of G. bengalensis from Pakistan to the EU-28 comprised 10 wild-sourced scientific

specimens exported in 2013, as reported by Pakistan. Direct exports of G. bengalensis from Pakistan to

countries other than the EU-28 comprised very low quantities of wild-sourced feathers, skeletons and

scientific specimens exported in 2006-2007 and 2015 (Table 2).

There has never been any reported indirect trade in G. bengalensis originating from Pakistan to the EU-

28.

Table 2: Direct exports of Gyps bengalensis from Pakistan to the rest of the world (RoW), 2006-2015. No trade was reported 2008-2014. All trade was wild-sourced for scientific purposes. Quantities have been rounded to one decimal place, where appropriate.

Importer Term Unit Reported by 2006 2007 2015

RoW feathers - Importer 200

Exporter 200

skeletons - Importer

Exporter 3

specimens L Importer 0.1

Exporter

- Importer

Exporter 10 75

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 03/08/2016.

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Conservation status

Gyps bengalensis is a medium-sized vulture with a range that was historically described as extending

across the Indian subcontinent to south Viet Nam and the Malay Peninsula (Ali and Ripley, 1968),

generally in temperate areas, up to 2600 m above sea level (Robson, 2015).

The species is considered to be highly social with a tendency to breed in colonies, the density of which

depends upon the suitability of surrounding habitat (BirdLife International, 2015). They feed in large

aggregations, scavenging the soft tissues of large mammals, primarily ungulates (Pain et al., 2003). For

this reason, G. bengalensis frequent areas near human habitation (Inskipp and Inskipp, 1991; Ali and

Ripley, 1968).

G. bengalensis was once described as the most abundant species of vulture on the Indian subcontinent

(Ali and Ripley, 1968), and was considered the most abundant bird of prey in the world until declines in

the early 20th century (BirdLife International, 2008). A rapid reduction in G. bengalensis numbers was

reportedly a consistent finding in all populations in all studies across the species range (Prakash et al.,

2003; Gilbert et al., 2004; 2006). The species has subsequently been categorised by the IUCN as Critically

Endangered reflecting the extremely high risk of extinction in the immediate future (BirdLife

International, 2001). In 2016 the global population was estimated to be between 3500 and 15 000

individuals (BirdLife International, 2016a). The species continues to decline rapidly and extinction was

noted to be a real possibility (Pain et al., 2008).

The primary threat to the species in Southeast Asia was noted to be the demise of large ungulate

populations owing to over-harvesting and improvements in animal husbandry resulting in a lack of

carcasses (BirdLife International, 2008). On the Indian subcontinent, the decline of G. bengalensis was

considered to be a direct result of individuals feeding on the carcasses of animals treated with the non-

steroidal anti-inflammatory drug (NSAID) diclofenac, which causes renal failure, visceral gout, and

eventually death (Oaks et al., 2004; Green et al., 2006; Arshad et al., 2009; Cuthbert et al., 2016; BirdLife

International, 2015). Mortality has been reported to be higher amongst males, skewing the population

sex ratio and hence the breeding potential of the population (Gilbert et al., 2006). Further threats

contributing to the decline of this species include habitat destruction, food scarcity, and human

persecution (BirdLife International, 2001).

Bangladesh: Birdlife International (2015) considered G. bengalensis to be regionally extinct in

Bangladesh. Monitoring surveys of suitable habitat throughout Bangladesh in 2011-2012 recorded the

total population to be 816 individuals. These surveys noted a drastic population decline of almost 60 per

cent between 2008 and 2012 (Khan and Monirul, 2013); the population declined from 1972 individuals in

2008-2009 to 1456 individuals in 2009-2010 and 991 in 2010-2011 (Khan and Monirul, 2013). The species

was considered common and widely distributed in Bangladesh in the 1990s (Harvey 1990; Thompson &

Johnson 1996 in Khan and Monirul, 2013).

The population decline between 2008 and 2012 was reported to be due to diclofenac poisoning and a

shortage of food (Khan and Monirul, 2013).

The government of Bangladesh reportedly signed the Regional Declaration on the Conservation of South

Asia Critically Endangered Species in May 2012 (Khan and Monirul, 2013). Khan and Monirul (2013)

reported that awareness programmes had been conducted to educate local people on actions to help

vultures. It was reported that provisional “Vulture Safe Zones” were being established in Bangladesh

(Mukherjee et al. 2004 in Birdlife International, 2016b) which would provide a safe environment into

which captive-bred birds could be released (Bowden et al., 2012).

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Bhutan: In 1999, G. bengalensis was reported as common around the border towns of Phuntsholing

[south-western Bhutan] and less so around Samdrup Jongkhar [south-eastern Bhutan], with flocks of up

to 50 individuals roosting in plantation woodlands at the edge of these towns. Smaller numbers were

occasionally observed soaring at altitudes of approximately 1300 m above sea level near Deothang

[south-eastern Bhutan] (Bishop, 1999). The species has also been recorded in Harachlu (and in Royal

Manas National Park [southern Bhutan] in 1993 (Inskipp and Inskipp 1993).

According to BirdLife International (2015), G. bengalensis still occurs in Bhutan. No further information

on population status or range was identified. G. bengalensis was not listed on Schedule I of the Forest

and Nature Conservation Act 1995 which prohibits killing, capture, collection and possession without a

permit (Royal Government of Bhutan, 1995).

Brunei Darussalam: G. bengalensis is a vagrant of Brunei (BirdLife International, 2016a). Two

individuals of this species were reportedly recorded in Brunei in 1977 although it is possible that this

record pertains to the Himalayan Griffon, Gyps himalayensis (Myers, 2016).

Cambodia: G. bengalensis was reported to occur throughout most of the country (Clements et al., 2012)

although viable populations of G. bengalensis were reported to be mainly in the north (Clark et al., 2016).

Clements et al. (2012) estimated the minimum population size by carrying out counts at supplemental

feeding stations at seven sites in Cambodia in 2004, and every year between 2006 and 2011. An increase

in the minimum population size was recorded between 2004 and 2011 of over 100 per cent from 90 to

183 individuals (Clements et al., 2012). Numbers were found to be greatest at the two northerly sites

(Preah Vihear Protected Forest and Siempang), stable at the central sites (Seasan and Lomphat Wildlife

Sanctuary) and declining in the southern and eastern sites (Mondulkiri Protected Forest and Phnom

Prich Wildlife Sanctuary (Clements et al., 2012). Small areas of north-eastern and northern Cambodia

hold relict populations, with some extension into adjacent parts of Lao PDR and Vietnam (Pain et al.,

2003). Their global significance in this country, as with Myanmar, lies in the fact that diclofenac is not in

use (Hla et al., 2011).

Principal threats to G. bengalensis populations in Cambodia were reported to be accidental poisoning as

a consequence of local hunting and fishing, and hunting or capture for traditional medicine (Clements

et al., 2012). The species was also considered threatened by lack of food availability (S. Mahood in litt.

2012 in Birdlife International, 2015).

G. bengalensis was listed as a ‘rare’ species on Cambodia’s list of protected species in the Law on

Forestry, a designation restricted to species with low population densities that may be at risk of

extinction in the wild (Cambodian Ministry of Agriculture Forestry and Fisheries, 2002a). Article 49 of

Chapter 10 of the Law on Forestry prohibits the following actions for rare or endangered species without

a permit: to harrass or harm the species or its habitat, hunt, trap or poison, possess, transport or trade

(Cambodian Ministry of Agriculture Forestry and Fisheries, 2002b).

China: MaMing and Xu (2015) reported G. bengalensis in the west and south-west of Yunnan Province

[southern China], and reported that the population in China was estimated to be 100-200 individuals.

P. Alstöm in litt. (2000 in Birdlife International, 2001) noted that there were “apparently no recent

records of the species in China” and in 2001, the status of the species was noted to be unknown but likely

to be scarce or rare (Birdlife International, 2001). However, Clark et al. (2016) reported that the species

was “probably extinct in Yunnan” and BirdLife International (2015) reported that the species may be

extinct from southern China.

The species was noted to be threatened by NSAID poisoning and a lack of safe food (MaMing and Xu,

2015). MaMing and Xu (2015) also reported that vultures were reportedly killed for their feathers, and

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threatened by power grids, lack of food, capture for zoos and traditional medicine, but did not specify

that these threats affected G. bengalensis (MaMing and Xu, 2015).

Islamic Republic of Iran (hereafter referred to as Iran): The current status of G. bengalensis in Iran

was reported to be unknown (Clark et al., 2016). Hollom et al. (1988 in Birdlife International 2001) noted

that the species was formerly distributed in the south-east, but in 2001, the range was considered

unknown (Birdlife International, 2001). Birdlife International (2001) noted that the only records of the

species in Iran from 1960 onwards were in Gandu (Bahu Kalat) Protected Area in 1972 and 25 km south-

east of Minab in 1971 (both from D. A. Scott in litt. 2000 in Birdlife International, 2001).

No information on the conservation status or management of this species in Iran was identified.

Lao People’s Democratic Republic (hereafter referred to as Lao PDR): G. bengalensis was noted to

have declined greatly, having once occurred throughout Lao PDR but becoming restricted to the

southern parts of Champasak Province in south-western Laos and neighbouring Attapeu Province in the

south-east of the country (Thewlis et al., 1998). Robson (2015) described the species as being resident in

the south of Lao PDR.

No records of specific threats to the species were found but general threats to birds in Lao PDR include

logging, large scale forest clearance and fragmentation for subsistence and commercial purposes, and

widespread unrestricted hunting (Thewlis et al., 1998).

G. bengalensis is found within the List of Restricted Wild and Aquatic Life Species (List I) (Lao People’s

Democratic Republic, 2003). This category refers to rare and near extinct wild and aquatic life with high

value and special socio-economic and environmental importance for the country. These species are

strictly managed and any activity relating to them requires approval from the Ministry of Agriculture

and Forestry (Lao People’s Democratic Republic, 2003).

Malaysia: The species has been described as historically found in northern Peninsula Malaysia (Robson,

2015), and formerly a widespread resident along the full length of Peninsular Malaysia before 1999, when

it was considered a rare non-breeding visitor (Wells, 1999 in Birdlife International, 2001). G. bengalensis

was described as being regionally extinct in 2015 (BirdLife International, 2015). Clark et al. (2016) also

reported that G. bengalensis was probably extinct in Malaysia.

Myanmar: G. bengalensis is reportedly resident in north and west Myanmar (Robson, 2015). The species

has been considered to occur only in sub-optimal habitat on the edge of its range, having been

completely lost from its strongholds in central and southern lowland areas including Minbu District,

Yangon, Sittang Basin and Arakhan State (Hla et al., 2011).

Clark et al. (2016) reported that the population was believed to “probably be in the low hundreds of

individuals”. Eight young were reported to have fledged in 2011 from a small colony in Kachin State

[northern Myanmar], which was “apparently the first confirmed successful breeding in Myanmar since

1932” (Clark et al., 2016).

Hla et al. (2011) carried out surveys for vultures at sites that had records within the last 12 years.

Supplemental feeding stations were used at sites in Kachin State, Sagaing Division, Shan State and Chin

State between 2006 and 2007 and the number of vultures counted (Hla et al., 2011). Based on these

surveys, a minimum population of 62 individuals was estimated in Myanmar (Hla et al., 2011).

It was noted that the species faced continual decline primarily due to food limitation as well as being

threatened by destruction of nesting colonies, poisoning, and hunting for their wings and meat (Hla et

al., 2011).

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The family Accipitridae, including all vultures, are listed as “completely protected” in Myanmar on

Article 15A on the Protection of Wildlife, Wild Plants and Conservation of Natural Areas Law (Ministry

of Forestry Myanmar, 1994). Act 37 of this law prohibits killing, hunting, wounding, possessing, selling

and transporting of completely protected wildlife without permission (Ministry of Forestry Myanmar,

1994).

Nepal: G. bengalensis was described as the most common and widespread vulture resident in Nepal up

to approximately 1000 m above sea level, with fewer individuals found in the Kathmandu Valley at

altitudes of 1370 m above sea level and less frequently up to 1800 m above sea level (Inskipp and Inskipp,

1991). This species is now considered a patchily distributed resident, rare in the centre, rare and very

local in the east and locally frequent in the west (Inskipp et al., 2016).

Populations have reportedly declined significantly in lowland Nepal, by 14 per cent a year between 2002

and 2011 (Chaudhary et al., 2012). Baral et al. (2004) reported maximum counts of 150 birds per day in

Koshi Tappu Wildlife Reserve [eastern Nepal] in 2000, and only 22 birds per day in 2003, reflecting an

85.3 per cent reduction. The number of active nests during this time declined by 78.5 per cent and

annual adult mortality was calculated to be 26.2 per cent suggesting that the population was

diminishing rapidly (Baral et al., 2004).

Prakash (2012) reported that the rate of decline of G. bengalensis in Nepal appears to have slowed and

may even have reversed, coinciding with partially effective efforts to reduce veterinary use of diclofenac

(Prakash et al., 2012). However, Baral et al. (2013) stated that populations in Ramur in southern Nepal

were in danger of disappearing within two decades (Baral et al., 2013).

G. bengalensis populations are threatened with forest degradation, pesticide use, disturbance to

breeding, roosting and feeding areas and the continued use of veterinary diclofenac (Inskipp et al., 2016).

The species was not listed on Schedule 1 of the National Parks and Wildlife Conservation Act, 2029

(1973), which prohibits hunting of protected species (Government of Nepal, 1973). The government of

Nepal reportedly signed the Regional Declaration on the Conservation of South Asia Critically

Endangered Species in May 2012 (Khan and Monirul, 2013).

A captive breeding facility within Nepal was noted to have 14 individuals in 2008 (Pain et al., 2008). It

was reported that provisional “Vulture Safe Zones” were being established in Nepal (Mukerjee et al.,

2004 in Birdlife International, 2016b) which would provide a safe environment into which captive-bred

birds could be released (Bowden et al., 2012).

Pakistan: In 2000, G. bengalensis breeding sites at Dholewala, Toawala and Changa Manga in Punjab

Province in Pakistan [eastern Pakistan] were reported to be the largest known colonies across the

species’ range (Gilbert et al., 2006). However, populations have declined significantly in Pakistan since

the early 1990s (BirdLife International, 2008). High mortality rates and population declines were noted

in Dholewala and Changa Manga, both in Punjab Province in 2000-2001 (Gilbert et al., 2002), leading to

extinction of both populations by 2004 (Gilbert et al., 2006). Breeding colonies in Toawala [Punjab

Province] decreased from 22.24 birds/km in 2006 to 9.39 birds/km in 2007 (Arshad et al., 2009). An

annual population decline of 50 was reported for breeding pairs of G. bengalensis in nesting colonies in

the Punjab Province of Pakistan between 2000 and 2003 (Green et al., 2004; Gilbert et al., 2004, 2006)

and surveys of 23 known colonies in 2006 reported a total of only 37 breeding pairs (Murn et al., 2008).

The primary threat to the species in Pakistan is diclofenac poisoning coupled with rapid shifts in

agrarian socioeconomic patterns which have reduced the availability of carcasses, so much so that food

limitation may prevent vulture populations from recovering to pre-decline numbers (Abbas et al., 2013).

All members of the family Accipitridae, including G. bengalensis, are listed on the third schedule of the

Baluchistan Wildlife Protection Act (1974), which prohibits the hunting, killing or capturing of this

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species (Government of Baluchistan, 1974). The government of Pakistan reportedly signed the Regional

Declaration on the Conservation of South Asia Critically Endangered Species in May 2012 (Khan and

Monirul, 2013).

In 2008, there were reportedly 11 individuals in a captive breeding centre in the country (Pain et al.,

2008). As in Nepal, it was reported that provisional “Vulture Safe Zones” were being established in

Pakistan (Mukerjee et al., 2004 in Birdlife International, 2016b) which would provide a safe environment

into which captive-bred birds could be released (Bowden et al., 2012).

Russian Federation: G. bengalensis was reported to be a vagrant of the Russian Federation (BirdLife

International, 2015).

No further information on this species in the Russian Federation was identified.

Thailand: G. bengalensis was described as resident in Thailand (BirdLife International, 2015), specifically

in the south of the country (Robson, 2015). Birdlife International (2001) noted that the species had

previously been resident throughout the country but that it was close to extinction in 2001.

G. bengalensis was specified as a protected species of wildlife under the “Wild Animal Reservation and

Protection Act 1992”, making it strictly prohibited to hunt, remove from the wild, or possess for trade

any individuals or their nests (National Wild Animal Reservation and Protection Committee, 1992).

Viet Nam: In 2000, G. bengalensis was noted to be almost extinct in South Annam and Cochinchina

[southern Viet Nam] where it had formerly been resident (Robson et al., 1990 in Birdlife International,

2001). The species was once described as the commonest vulture in southern Viet Nam (Wildash, 1968).

However, Thewliss et al. (1998) considered the species “almost extinct” in Viet Nam. Brickle et al. (1998)

recorded sightings of single birds in Dak Lak Province [central Viet Nam] in 1998. The species was not

recorded as part of a national survey between 1989 and 1990 (Robson et al., 1990 in Birdlife

International, 2001).

No further information on the conservation status or management of this species in Viet Nam was

identified.

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Pain, D.J., Bowden, C.G.R., Cunningham, A.A., Cuthbert, R., Das, D., Gilbert, M., Jakati, R.D., Jhala, Y., Khan, A.A., Naidoo, V. et al. 2008. The race to prevent the extinction of south Asian vultures. Bird Conservation International, 18: S30–S48.

Pain, D.J., Cunningham, A.A., Donald, P.F., Duckworth, J.W., Houston, D.C., Katzner, T., Parry-Jones, J., Poole, C., Prakash, V., Round, P. et al. 2003. Causes and effects of temporospatial declines of Gyps vultures in Asia. Conservation Biology, 17(3): 661–671.

Prakash, V., Bishwakarma, M.C., Chaudhary, A., Cuthbert, R., Dave, R., Kulkarni, M., Kumar, S., Paudel, K., Ranade, S., Shringarpure, R. et al. 2012. The population decline of Gyps vultures in India and Nepal has slowed since veterinary use of diclofenac was banned. PLoS ONE, 7(11).

Prakash, V., Pain, D.J., Cunningham, A.A., Donald, P.F., Prakash, N., Verma, A., Gargi, R., Sivakumar, S. and Rahmani, A.R. 2003. Catastrophic collapse of Indian white-backed Gyps bengalensis and long-billed Gyps indicus vulture populations. Biological Conservation, 109: 381–390.

Robson, C. 2015. Birds of South-East Asia. Bloomsbury Publishing Ltd, London, UK and New York, US. 304 pp. Robson, C. R., Eames, J. C., Newman, M., Nguyen Cu and Truong Van La. 1990. Forest bird surveys in Vietnam

1989/90: final report. Unpublished report to the International Council for Bird Preservation. Royal Government of Bhutan 1995. Forest and Nature Conservation Act of Bhutan. Available at:

http://www.asianlii.org/bt/legis/laws/fancaob1995409/ [Accessed 16 September 2016] Thewlis, R.M., Timmins, R.J., Evans, T.D. and Duckworth, J.W. 1998. The conservation status of birds in Laos: a

review of key species. Bird Conservation International, 8: 47. Thompson, P. M. & Johnson, D. L. 1996. Birding in Bangladesh – a guide to birdwatching sites and a checklist of

birds. Dhaka: unpublished report. Wells, D. R. 1999. The birds of the Thai-Malay Peninsula, 1. London: Academic Press. Wildash, P. 1968. Birds of South Vietnam. First. Charles E. Tuttle Company Inc. 59 pp.

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Bugeranus carunculatus

GRUIFORMES: GRUIDAE

Bugeranus carunculatus II/B

Trade patterns

Bugeranus carunculatus was listed in Appendix II on 01/08/1985 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the family listing for Gruidae.

South Africa has submitted annual reports for the years 2006-2014, but has not yet submitted an annual

report for 2015. South Africa has never published an annual export quota for B. carunculatus.

Direct exports of B. carunculatus from South Africa to the EU-28 2006-2015 comprised very low

quantities of wild-sourced (20) and source F (0.03l) scientific specimens exported in 2012, as reported by

South Africa. Direct trade in B. carunculatus from South Africa to countries other than the EU-28 2006-

2015 comprised one wild-sourced scientific specimen exported in 2008, as reported by South Africa and

the importer.

There has never been any reported indirect trade in B. carunculatus originating from South Africa to the

EU-28.

Conservation status

Bugeranus carunculatus is endemic to Africa, ranging from Ethiopia to Angola and South Africa

(Archibald et al., 2016). The species inhabits large wetlands, preferably in riparian floodplains (Burke,

1996; Archibald et al., 2016), grassland and agricultural land (McCann and Benn, 2006) and was reported

SYNONYMS: Ardea carunculata, Grus carunculatus

COMMON NAMES: Wattled Crane (EN), Grue Caronculée (FR), Grulla Carunculada (ES)

RANGE STATES: Angola, Botswana, Democratic Republic of the Congo, Ethiopia, Guinea Bissau (distribution uncertain), Lesotho, Malawi, Mozambique, Namibia, South Africa, Swaziland (extinct), United Republic of Tanzania, Zambia, Zimbabwe

UNDER REVIEW: South Africa

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from South Africa applied on 21/11/1998 and last confirmed on 28/05/2015.

Current Article 4.6(b) import suspension for wild specimens from the United Republic of Tanzania applied on 10/05/2006 and last confirmed on 28/05/2015.

Current no opinion iii) for wild specimens (opinion originally formed for Grus carunculatus) from Angola, Botswana, Democratic Republic of the Congo, Ethiopia, Guinea Bissau, Lesotho, Malawi, Mozambique, Namibia, Swaziland, Zambia and Zimbabwe formed on 25/06/2004.

IUCN: Vulnerable

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to be the most dependent on wetlands of all African cranes (Archibald et al., 2016). It is considered non-

migratory, but irregularly nomadic depending on availability of water (Archibald et al., 2016).

B. carunculatus was considered a specialised breeder in shallow wetlands dominated by sedge, breeding

above altitudes of 2000 m above sea level, but generally occurring below 1000 m otherwise (Archibald et

al., 2016). Sexual maturity was reported to be at approximately seven to eight years of age (Coverdale

and McCann, 2003; BirdLife International, 2013) with a clutch size of one to two eggs (usually one)

(Archibald et al., 2016), although, only one chick is raised (McCann et al., 2001). B. carunculatus was

considered to be “extremely sensitive” to disturbance, with repeated disturbance potentially resulting in

a breeding area being abandoned (Tarboton et al., 1987 in McCann et al., 2001). The species was noted to

be more difficult to breed in captivity than other cranes (Archibald et al., 2016).

B. carunculatus was categorised as Vulnerable by the IUCN on the basis of a small population that

appears to have undergone a rapid decline, which is projected to continue (BirdLife International, 2013).

Three disjunct populations were reported to exist (Jones et al., 2006; Beilfuss et al., 2007), with the

majority of birds in a large south-central population in the floodplain systems of southern Africa’s large

river-basins (especially the Kafue, Okavango and Zambezi) and two smaller isolated populations in

Ethiopia and South Africa (Beilfuss et al., 2007). Historically, the species was reported to have been more

abundant and more widely distributed across Southern Africa (Burke, 1996).

The total population size was estimated to be between 6000 - 8000 individuals (Archibald et al., 2016),

equating to approximately 4000 - 5300 mature individuals (BirdLife International, 2013), having

undergone a significant decline since the mid-1980s to 1990s, when the global population was estimated

at 13 000 – 15 000 individuals (Archibald et al., 2016). The species was reported to have declined in nine

range states (Beilfuss et al., 2007), with the greatest losses reported to have occurred in South Africa

(Burke, 1996).

The main threats to the species were reported to be loss and degradation of wetlands (Burke, 1996;

BirdLife International, 2013; Archibald et al., 2016). Other threats were reported to include human

disturbance, poisoning and collision with utility lines (Archibald et al., 2016), as well as illegal removal of

eggs and chicks for international trade (Pittman, 2007).

In 1996, a conservation action plan for cranes was developed (Meine and Archibald, 1996), and in 2001,

the African Wattled Crane Programme (AWAC) was launched to monitor the status and threats to the

species in each range state and to support the development of conservation programmes for the

management of wetland systems (Beilfuss and Bento, 2003 in Beilfuss et al., 2007). Protected areas were

reported to have been established in several key wetlands within the species range, in particular in

Zambia, Namibia and Botswana (Burke, 1996; Archibald et al., 2016).

South Africa: The South Africa population of B. carunculatus was reported to be genetically isolated

from the other populations (Jones et al., 2006). It was reported that around 95 per cent of South Africa’s

population of B. carunculatus are located within KwaZulu-Natal Province [eastern South Africa] (Smith,

2015), therefore conservation efforts were noted to have focussed on this region (Smith et al., 2012).

Annual crane aerial surveys were reported to have been carried out in KwaZulu-Natal since the early

1990s (Smith et al., 2012; Smith, 2015). In 2007, the population of B. carunculatus in South Africa was

“accurately known to be 242 individuals”, including 80 breeding pairs based on direct counts (McCann

in litt. to Beilfuss et al., 2007). In 2010, the survey recorded 226 individuals and a stable and potentially

increasing population (Smith et al., 2012). In 2015, aerial surveys confirmed this trend, with

291 individuals recorded (the second highest recorded count since the aerial surveys began) representing

an increase of between 59-69 per cent since 2001 (Smith, 2015).

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Historically, B. carunculatus was reported to be widespread in South Africa, occurring in all four former

provinces (Burke, 1996; McCann et al., 2001), and extending south into western parts of the Cape

Province (Burke, 1996; Pittman, 2007). At the turn of the century, it was reported to occupy a “vastly

restricted” range in the eastern regions of South Africa, occurring as two main subpopulations - in the

Mpumalanga Highlands and KwaZulu-Natal [midlands to southern parts] (McCann et al., 2001), having

undergone a range reduction of 76 per cent from its historical distribution (McCann et al., 2001) and a

population decline of more than 35 per cent over two decades prior to the early 2000s (South African

Crane Working Group, 2000; Pittman, 2007). The species was listed as a ‘critically endangered’ species in

the list of threatened or protected species (Notice 255 of 2015) (Department of Environmental Affairs,

2015) that are protected under the National Environmental Management: Biodiversity Act 2004

(Government of South Africa, 2004). Furthermore, the 2014 Eskom Red Data Book of Birds of South

Africa, Lesotho and Swaziland also categorised the species as ‘critically endangered’ (BirdLife

International, 2015).

Loss and degradation of wetland habitats was reported to pose the main threat to the species in South

Africa (South African Crane Working Group, 2000). Other threats were reported to include powerline

collisions, burning of wetlands and capture of chicks for the international bird trade (South African

Crane Working Group, 2000). These threats were reported to be further compounded by the species low

reproductive rate and dependence on wetland habitats (Pittman, 2007).

Conservation efforts undertaken in South Africa were reported to include legal protection,

communication of appropriate habitat conservation practices to private landowners, marking and

relocation of utility lines, and education and awareness programmes (Burke, 1996; Archibald et al.,

2016). It was reported that several nature reserves have been established for the protection of breeding

pairs and their habitats (Burke, 1996) and the species was reported to have triggered the criteria for a

number of Important Bird Areas (in Mpumalanga, KwaZulu-Natal and Free State) (BirdLife

International, 2016).

In 2000, a National Crane and Habitat Action Plan was published (South African Crane Working Group,

2000). Furthermore, due to concerns over the species decline and its potential genetic uniqueness

(McCann et al., 2001), in 2001, a Population and Habitat Viability Assessment (PHVA) workshop was

held, which recommended the creation of a captive breeding and supplementation programme

(Pittman, 2007). Subsequently, the Wattled Crane Recovery Program was formed (Pittman, 2007). It was

reported that the species is legally protected by the Provincial Nature Conservation Ordinances in South

Africa (in the four former provinces) (Burke, 1996) which prohibited interference with nests, eggs, or

chicks, keeping cranes in captivity, or capturing, injuring or killing any individuals without a permit

from the local authority (Burke, 1996; Department of Environmental Affairs, 2015).

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References

Archibald, G.W., Meine, C.D. and Garcia, E.F.J. 2016. Wattled Crane (Bugeranus carunculatus). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (Ed.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona.

Beilfuss, R.. and Bento, C. 2003. Water, wetlands, and Wattled Cranes: a regional monitoring and conservation program for southern Africa. In: Bernard, T., Mosepele, K. and Ramberg, L. (Eds.). Proceedings of the International Conference on Environmental Monitoring of Tropical and Subtropical Wetlands, 4–7 December 2002. Okavango Research Centre, Maun, Botswana. 47–56.

Beilfuss, R.D., Dodman, T. and Urban, E.K. 2007. The status of cranes in Africa in 2005. Ostrich - Journal of African Ornithology, 78(2): 175–184.

BirdLife International 2013. Bugeranus carunculatus. The IUCN Red List of Threatened Species 2013 Available at: http://www.iucnredlist.org. [Accessed: 23 August 2016].

BirdLife International 2016. Species Factsheet: Bugeranus carunculatus. Available at: http://www.birdlife.org/. [Accessed: 23 August 2016].

Burke, A. 1996. Wattled crane (Bugeranus carunculatus). In: Meine, C.D. and Archibald, G.W. (Eds.). The cranes: status survey and conservation action plan. IUCN/SSC Crane Specialist Group, Gland, Switzerland and Cambridge, UK. 76–88.

Coverdale, B.M. and McCann, K.I. 2003. Breeding age and pair formation of Wattled Cranes, Bugeranus carunculatus, in the wild. Ostrich, 74(3–4): 226–227.

Department of Environmental Affairs 2015. Notice 255 of 2015. National Environmental Management: Biodiversity Act, 2004 (Act No. 10 of 2004). 284 pp. Available at: http://faolex.fao.org/docs/pdf/saf146021.pdf. [Accessed 23 August 2016].

Government of South Africa 2004. National Environmental Management: Biodiversity Act, 2004 (Act 10 of 2004). Jones, K.L., Rodwell, L., McCann, K.I., Verdoorn, G.H. and Ashley, M. V. 2006. Genetic conservation of South

African wattled cranes. Biological Conservation, 127(1): 98–106. McCann, K., Burke, A., Rodwell, L., Steinacker, M. and Seal, U.S. (Eds.) 2001. Population and habitat viability

assessment for the wattled crane (Bugeranus carunculatus) in South Africa. Final workshop report. Apple Valley, Minnesota, USA. 169 pp.

McCann, K.I. and Benn, G.A. 2006. Land use patterns within wattled crane (Bugeranus carunculatus) home ranges in an agricultural landscape in KwaZulu-Natal, South Africa. Ostrich - Journal of African Ornithology, 77(3–4): 186–194.

Meine, C.D. and Archibald, G.W. 1996. The cranes: status survey and conservation action plan. IUCN/SSC Crane Specialist Group, Gland, Switzerland and Cambridge, UK.

Pittman, J.M. 2007. Update on the Wattled Crane Recovery Program, South Africa. Re-introduction News, 26: 17–18. Smith, T. 2015. Crane counts on the up in KwaZulu-Natal, South Africa. E-newsletter of the EWT’s African Crane

Conservaton Programme, (December 2015): 8–9. Smith, T., Craigie, J. and McCann, K. 2012. Summary of the 2010 annual KZN Crane aerial survey. Indwa - Journal of

African Crane Research and Conservation, 8: 26–34. South African Crane Working Group 2000. National crane and habitat action plan. South Africa. 19 pp. Tarboton, W.R., Kemp, M.I. and Kemp, A.C. 1987. Birds of the Transvaal. Gutenberg Book Printers, Pretoria West.

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Agapornis nigrigenis

PSITTACIFORMES: PSITTACIDAE

Agapornis nigrigenis II/B

Taxonomic Note

This review follows the CITES Standard Reference which recognises Agapornis nigrigenis as a distinct

species (Dickinson, 2003). However, Collar, (2016) noted that A. nigrigenis is sometimes treated as a

subspecies of A. lilianae and can be considered to form a species-group with Agapornis lilianae,

Agapornis fischeri and Agapornis personatus (Collar, 2016).

Trade patterns

Agapornis nigrigenis was listed in Appendix II on 06/06/1981 and in Annex B of the EU Wildlife Trade

Regulations on 01/06/1997 as part of the order listing for Psittaciformes.

There has never been any reported trade in A. nigrigenis from Botswana or Zambia to the EU-28 or

elsewhere. These countries have also never produced export quotas for the species.

Namibia: Namibia has submitted annual reports for the years 2006-2014 but has not yet submitted

annual reports for 2007 or 2015. Namibia has never published an annual export quota for A. nigrigenis.

There was no direct trade in A. nigrigenis from Namibia to the EU-28 reported over the period 2006-

2015, or prior to this. Direct trade in A. nigrigenis from Namibia to countries other than the EU-28 2006-

2015 consisted of 8 live, captive-bred individuals exported for breeding purposes in 2012, as reported by

Namibia.

There has never been any reported indirect trade in A. nigrigenis originating from Namibia to the EU-28.

Zimbabwe: Zimbabwe have submitted annual reports for the years 2006-2014, but have not yet

submitted an annual report for 2015. Zimbabwe has never published an annual export quota for

A. nigrigenis.

There was no direct trade in A. nigrigenis from Zimbabwe to the EU-28 reported over the period 2006-

2015, however, low levels of trade were reported prior to this. Direct trade in A. nigrigenis from

SYNONYM: Agapornis lilianae nigrigenis

COMMON NAMES: Black-cheeked Lovebird (EN), Perruche à Joue Noire (FR), Inseparable Cachetón (ES)

RANGE STATES: Botswana, Namibia, Zambia, Zimbabwe

UNDER REVIEW: Botswana, Namibia, Zambia, Zimbabwe

EU DECISIONS: Current Article 4.6(b) import suspension for wild specimens from Botswana, Namibia, Zambia and Zimbabwe first applied on 22/12/1997 and last confirmed on 28/05/2015.

IUCN: Vulnerable

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Zimbabwe to countries other than the EU-28 2006-2015 consisted of 20 live, captive-bred individuals

exported for commercial purposes in 2007, as reported by Zimbabwe and the EU-28.

There has never been any reported indirect trade in A. nigrigenis originating from Zimbabwe to the EU-

28.

Conservation status

Agapornis nigrigenis is a small parrot, reported to have a restricted (Collar, 2016) and localised range

(Warburton and Perrin, 2005a), occurring in south-west Zambia (Dickinson and Remsen Jr, 2013; Collar,

2016), with a disjointed distribution between the River Kafue and the River Zambezi (Dodman et al.,

2000; Collar, 2016). The species presence has also been reported from north-western Zimbabwe, extreme

north-eastern Namibia and northernmost Botswana (Juniper and Parr, 1998; Forshaw, 2010). However,

the status of the species outside of Zambia was reported to be historically confusing (Warburton, 2003)

and reports from Botswana, Namibia and Zimbabwe were considered to be unconfirmed (Warburton,

2003; Collar, 2016).

A. nigrigenis was reported to inhabit mopane woodland with permanent standing water (Dodman et al.,

2000), at elevations of 600-1000 m above sea level (Juniper and Parr, 1998). While the species was

reported to be highly forest dependent (Collar, 2016), it was also reported to spread into crop fields to

forage “causing some damage” (Juniper and Parr, 1998).

Warburton (2003) studied the species in Zambia and reported that most of the pairs studied raised one

clutch per breeding cycle. Clutch sizes of between of two to eight have been recorded in captivity

(J. Boomker, D.V.D. Hofemeyer, U. Künzel, L. Lamke, B. Povisen. G. Scopes and S. Waters pers. comm.

in Warburton, 2003) and a maximum lifespan of almost 14 years has been reported (Young et al., 2012).

A. nigrigenis was categorised as Vulnerable by the IUCN on the basis of a small population that was

undergoing a continuing decline due, principally, to the gradual desiccation of water bodies within a

highly localised range (BirdLife International, 2013). According to Warburton (2003), the species

underwent a severe population decline in the 1920s and has not recovered since, although Sinclair and

Ryan (2010) considered the species locally common within its small range. Juniper and Parr (1998)

reported that the species was formerly common within a restricted range but, in 1998, was considered

local, uncommon and under serious threat. On the basis of surveys in 1994, the population size was

estimated at approximately 10 000 individuals (Dodman et al., 2000; BirdLife International, 2016b). Due

to suspected declines in the populations since then, this population estimate has been updated to

between 2500 and 9999 mature individuals, equating to approximately 3500 - 15 000 individuals

(BirdLife International, 2016b).

Water availability was reported to be a limiting factor for the species (Warburton and Perrin, 2005b) and

gradual desiccation of its habitat was reported to be the main threat (Dodman et al., 2000), with a range

reduction and increasing dependence on artificial water sources reported as a result (Warburton and

Perrin, 2005b). An assessment of species vulnerability to climate change found A. nigrigenis to be highly

vulnerable to indirect impacts (Segan et al., 2013).

Heavy exploitation of wild populations for the cage-bird trade from the 1920s – 1960s was reported to

have been a main cause of the species decline (Dodman et al., 2000; BirdLife International, 2013). It was

reported that the species appears to be susceptible to trapping (Juniper and Parr, 1998), due to its social

habits and dependence on water (Warburton, 1999), and highly vulnerable [to trapping] due to its

localisation (Dodman et al., 2000). It was noted that any international demand would be eagerly met

(Warburton and Perrin, 2005c) and both Wilkinson (1998) and Warburton (2003) cautioned that

resumption of the capture of wild birds for trade could pose a significant threat to the species survival.

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Botswana: The species occurrence has been reported from the northernmost tip of Botswana (Juniper

and Parr, 1998; Forshaw, 2010), however, these reports were considered unconfirmed by Dowsett and

Forbes-Watson (1993 in Wilkinson, 1998) and Collar (2016). Furthermore, Dodman et al. (2000) noted

that the species’ status in Botswana was confused by the presence of feral lovebirds.

The species was included in a list of globally threatened species found in Botswana in 1988 (Hannah et

al., 1988) and in 2004 (BirdLife International, 2004 in Kayombo et al., 2014). It was also included in the

country’s First National Report to the CBD in 1998 (Government of Botswana, 1998), but not in any CBD

reports since.

Namibia: The species has been reported to occur in the extreme north-east of Namibia (Juniper and

Parr, 1998; Forshaw, 2010), although Dowsett and Forbes-Watson (1993 in Wilkinson, 1998) and Collar

(2016) considered reports from Namibia to be unconfirmed.

The species’ presence was reported in the Caprivi region [extreme north-eastern Namibia], including on

Impalila Island (Juniper and Parr, 1998; Dodman et al., 2000) and in villages east of Katima Mulil

(Dodman et al., 2000). It was reported that the species may be an occasional visitor to Namibia from

adjacent Zambia (Dodman et al., 2000; Leonard, 2001), probably occurring at times when crops are

ripening (Dodman et al., 2000). Dodman et al. (2000) noted that previous reports from eastern Caprivi

appeared to be genuine and were in need of further investigation, although the possibility that these

were feral birds was noted. Two populations of escaped birds were reported to persist at Mount Etjo

(near Omaruru) and Okaukuejo (in Etosha National Park) (Simmons et al., 2015).

Leppan (1944) reported a “plentiful flock” of A. nigrigenis in eastern Caprivi, although the credibility of

this record has been questioned (Benson and Irwin, 1967 in Warburton, 2003) and surveys in the area in

1994 and 1999 could not confirm its presence (Dodman, 1995 in Warburton, 2003). Warburton (2003)

considered it unlikely that a resident population of such a conspicuous species could have been

overlooked in the eastern Caprivi Strip or Impalila Island, and concluded that a single bird observed

near Katima Mulilo 1998 was likely to have been an escapee.

Simmons et al. (2015) considered the species to be ‘critically endangered’ in Namibia, on the basis that

although the current population is unknown, it probably consists of fewer than 50 individuals.

A. nigrigenis was included in the 2015 Red Data book of Namibian birds on the basis that the species is

occasionally sighted in Namibia and that it “once occurred regularly in north-eastern Namibia”

(Simmons et al., 2015). It was thought that more birds may appear in Namibia over the next one to two

decades as a result of conservation efforts in Zambia, and systematic surveys to determine population

levels were recommended (Simmons et al., 2015).

Threats to potential future populations of the species in Namibia were thought to include the parrot

trade and degradation of woodlands (Simmons et al., 2015).

Zambia: A. nigrigenis was considered to be virtually endemic to Zambia (Wilkinson, 1998; Warburton,

2003; Sinclair and Ryan, 2010).

A. nigrigenis was reported to have a highly localised and clumped distribution in south-west Zambia

(Warburton, 2003), mainly occurring between the Zambezi and Kahe rivers (Dodman et al., 2000;

Warburton, 2003). Its area of occupancy was estimated at 2500 km2, within an area of mopane woodland

estimated at 4500 km2. Tw0 distinct subpopulations were reported to exist (Dodman et al., 2000;

Warburton, 2003). The northern population was reported to occur in suitable habitat along the length of

the Nanzhila River and the southern population centred around the Sichifulo River, ranging between

the river systems of the Simatanga, the Ngweze and the Machile (Dodman et al., 2000). In 1994, the

population size was estimated at 10 000 birds (Dodman et al., 2000), with 3800 in the northern

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subpopulation and 6200 in the southern subpopulation (Dodman, 1995 in Wilkinson, 1998). Population

declines and local extinctions were noted by Dodman et al. (2000), and Warburton (2003) considered it

likely that the range of A. nigrigenis was further decreasing.

Between the 1920s and 1960s, it was reported that the species was trapped excessively, principally for the

pet trade, although by 2000 this trade was considered uncommon, with a few isolated incidents reported

(Dodman et al., 2000). The major threat to the species was noted to be desiccation, due to climate

change (Dodman et al., 2000; Warburton, 2003). Other threats were reported to include the potential

resumption of illegal trade, killing for local consumption and possibly killing to prevent crop damage

(Dodman et al., 2000).

The species was reported from two Important Bird Areas (IBAs): Kafue National Park and Machile

(which includes Machile Forest Reserve) (BirdLife International, 2016b). Machile was reported to be a

stronghold for A. nigrigenis, supporting approximately 5500 adults in 1998, which represented over half

of the known population (BirdLife International, 2016a). In 2013, it was noted that this IBA was under

serious pressure from a variety of threats and that immediate action was needed (BirdLife International,

2016a).

Trade in wild-caught A. nigrigenis was prohibited in Zambia in 1930, although it was reported that some

trade existed until the 1960s (Dodman, 1995 in Warburton, 2003). Given the species extremely localised

range and low population size, Warburton and Perrin (2005c) highly recommended the maintenance of

the trade ban. Warburton (2003) further noted that harvesting should not be recommended as part of a

current or future management strategy for the species.

Van den Abeele (2015) reported that in 2001 an educational project was held involving local schools,

residents and forest managers to support the species. As part of the project, protection laws were

introduced, including the prohibition to trade wild-sourced birds.

Zimbabwe: The species’ occurrence in Zimbabwe was considered to be unconfirmed (Collar, 2016) and

confused by the presence of feral birds (Warburton, 2003; Sinclair and Hockey, 2005; Sinclair and Ryan,

2010). It was considered locally extinct (Dowsett and Forbes-Watson, 1993 in Wilkinson, 1998; Evans and

Fishpool, 2001), if it ever occurred (Evans and Fishpool, 2001).

Reports of the species are confined to the north-west of the country (Juniper and Parr, 1998; Sinclair and

Hockey, 2005; Sinclair and Ryan, 2010), particularly Livingstone and Victoria Falls (Warburton, 2003),

including the “last reliable record” of the species at Victoria Falls in 1967 (C. Pollard pers. comm. in

Dodman et al. 2000). It was also reported as locally common 100 miles east of Victoria Falls along the

Zambezi (Winterbottom, 1952 in Warburton, 2003).

The status of A. nigrigenis in the country was reportedly confused by the presence of feral lovebirds,

particularly wild-caught birds for trade that may have escaped in the Victoria Falls and Livingstone areas

(Warburton, 2003). The species was considered not to occur naturally in these areas following interviews

with local bird guides and residents, the distance from naturally occurring populations, and the lack of

historical records (Warburton, 2003).

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Agapornis nigrigenis

References

Van den Abeele, D. 2015. Agapornis. Hispano Europea. Benson, C.W. and Irwin, M.P.S. 1967. A contribution to the ornithology of Zambia. Zambia Museum Papers, 1: 41–43. BirdLife International 2013. Agapornis nigrigensis. The IUCN Red List of Threatened Species. Version 2016.1.

Available at: http://www.iucnredlist.org/. [Accessed: 11 August2016]. BirdLife International 2016a. Important Bird and Biodiversity Area factsheet: Machile. BirdLife International 2016b. Species Factsheet: Agapornis nigrigenis. Available at: http://www.birdlife.org.

[Accessed: 15 August 2016]. BirdLife International 2004. Threatened Birds of the World. Lynx Edicions and BirdLife International, Barcelona and

Cambridge. Collar, N. 2016. Black-cheeked Lovebird (Agapornis nigrigenis). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A.,

de Juana, E. (Ed.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. Dickinson, E.C. 2003. The Howard and Moore complete checklist of the birds of the world. 3rd Edition. Christopher

Helm Publishers Ltd., London, UK. Dickinson, E.C. and Remsen Jr, J.V. 2013. The Howard and Moore Complete Checklist of the Birds of the World. 4th

edition, Volume 1 Non-Passerines. Aves Press, Eastbourne, United Kingdom. Dodman, T. 1995. Status and distribution of the Black-cheeked Lovebird Agapornis nigrigenis. 50 pp. Dodman, T., Katanekwa, V., Aspinall, D. and Stjernstedt, R. 2000. Status and distribution of the Black-cheeked

Lovebird, Zambia. Ostrich, 71(1–2): 228–234. Dowsett, R.J. and Forbes-Watson, A.D. 1993. Checklist of birds of the Afrotropical and Malagasy regions. Tauraco

Press, Liège, Belgium. Evans, M.I. and Fishpool, L.D.C. 2001. Zimbabwe. In: Important Bird Areas in Africa and Associated Islands: Priority

Sites for Conservation. Pisces Publications and BirdLife International, Cambridge. 1025–1042. Forshaw, J. 2010. Parrots of the World. A & C Black, London. 336 pp. Government of Botswana 1998. National report on measures taken to implement the Convention on Biological

Diversity. Bratislava, Republic of Slovakia. 77 pp. Hannah, L., Wetterberg, G. and Duvall, L. 1988. Botswana Biological Diversity Assessmenti. 110 pp. Juniper, T. and Parr, M. 1998. Parrots: a guide to the parrots of the world. Pica Press, Robertsbridge, UK. Kayombo, B., Tsheko, R., Mmolawa, K.B. and Khonga, E.B. 2014. Inventory of endangered flora and fauna in Bobirwa

and Kgalagadi districts of Botswana. Journal of Agriculture and Biodiversity Research, 3(7): 99–110. Leonard, P.M. 2001. Zambia. In: Important Bird Areas in Africa and Associated Islands: Priority Sites for

Conservation. Pisces Publications and BirdLife International, Cambridge. 1005–1024. Leppan, A.W. 1944. Birds of the Eastern Caprivi Zipel. Ostrich, 15(1): 26. Segan, D.B., Watson, J.E.M., Hole, D.G., Donatti, C.I., Zganjar, C., Martin, S., Mutu, K. and Bailey, N. 2013. A

Systematic Approach to Incorporate the Human Response into Climate Change Conservation Planning. 48 pp. Simmons, R., Brown, C.J. and Kemper, J. 2015. Black-cheeked lovebird Agapornis nigrigenis. In: Birds to watch in

Namibia: red, rare and endemic species. Ministry of Environment and Tourism and Namibia Nature Foundation, Windhoek. 46–47.

Sinclair, I. and Hockey, P. 2005. The larger illustrated guide to birds of southern Africa. Struik Publishers, Cape Town, South Africa.

Sinclair, I. and Ryan, P. 2010. Birds of Africa south of the Sahara. 2nd Ed. Struik Nature, Cape Town. 767 pp. Warburton, L. 1999. Black-cheeked lovebirds in the wild. Psittascene, 11(2): 8–10. Warburton, L.S. and Perrin, M.R. 2005a. Foraging behaviour and feeding ecology of the Black-cheeked Lovebird

Agapornis nigrigenis in Zambia. Ostrich, 76(3–4): 118–129. Warburton, L.S. and Perrin, M.R. 2005b. Conservation implications of the drinking habits of Black-cheeked

Lovebirds Agapornis nigrigenis in Zambia. Bird Conservation International, 15(4): 383–396. Warburton, L. and Perrin, M.R. 2005c. Roosting requirements and behaviour of the Black-cheeked Lovebird

Agapornis nigrigenis (Sclater 1906) in Zambia. Tropical Zoology, 18: 39–48. Warburton, L.S. 2003. The ecology and conservation biology of the Black-cheeked Lovebird Agapornis nigrigenis in

Zambia. University of Natal. 221 pp. Wilkinson, R. 1998. The conservation status of African parrots: A review for the World Parrot Trust - Part 2.

Psittascene, 10(4): 10–12. Winterbottom, J.M. 1952. Some birds of the Victoria Falls. The Bokmakierie, 4(1): 10–11. Young, A.M., Hobson, E.A., Bingaman Lackey, L. and Wright, T.F. 2012. Survival on the ark: life-history trends in

captive parrots. Animal Conservation, 15: 28–43.

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Gopherus agassizii

TESTUDINES: TESTUDINAE

Gopherus agassizii II/B

Taxonomic note

Gopherus agassizii was split in 2011 based on geographic distribution, with populations in the Sonoran

desert named as a new species, G. morafkai, while populations of the Colorado desert (California) and

populations of the Mojave desert north and west of the Colorado River remain G. agassizii (Murphy et

al., 2011). Murphy et al. (2011) was adopted as a Standard Reference for these two species at the 16th

Conference of the Parties to CITES.

Trade patterns

Gopherus agassizii was listed in Appendix II on 01/07/1975 as part of the genus listing for Gopherus spp.

and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997 as part of the family listing for

Testudinidae.

The United States has submitted annual reports for the years 2006-2014, but has not yet submitted an

annual report for 2015. The United States has never published an annual export quota for G. agassizii.

Direct exports of G. agassizii from the United States to the EU-28 2006-2015 comprised very low

quantities of wild-sourced carapaces, scales and shells exported for scientific purposes in 2010 (Table 1).

Direct trade in G. agassizii from the United States to countries other than the EU-28 2006-2015

primarily comprised low levels of wild-sourced specimens for scientific purposes in the period 2010-2013

(Table 1). In addition, there were two live individuals exported for personal purposes: one wild-sourced

individual in 2006 and one seized individual in 2011 (Table 1).

There has never been any reported indirect trade in G. agassizii originating from the United States to

the EU-28.

SYNONYMS: Gopherus polyphemus agassizii, Scaptochelys agassizii, Testudo agassizii, Xerobates agassizii, Xerobates lepidocephalus

COMMON NAMES: Desert Tortoise (EN), Gophère d’Agassiz (FR), Tortuga del Desierto (ES)

RANGE STATES: United States of America

UNDER REVIEW: United States of America

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

IUCN: Vulnerable (needs updating)

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Gopherus agassizii

Table 1: Direct exports of Gopherus agassizii from the United States to the EU-28 (EU) and the rest of the world (RoW), 2006-2015. No trade was reported 2007-2009, 2012, or 2014-2015. Quantities have been rounded to two decimal places, where appropriate.

Importer Term Unit Purpose Source Reported by 2006 2010 2011 2013

EU carapaces kg S W Importer

Exporter 1.37

scales kg S W Importer

Exporter <0.01

specimens kg S W Importer

Exporter 0.25

RoW live - P I Importer 1

Exporter

W Importer

Exporter 1

specimens - S W Importer

Exporter 284 1 2

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 03/08/2016.

Conservation Status

United States of America: Gopherus agassizii is a tortoise species reported to occur north and west of

the Colorado River in the Mojave Desert of California, Nevada, and south-western Utah, and in the

Colorado Desert in California (Murphy et al., 2011). Previously, the range of G. agassizii was considered

to reach as far south as Sonora and into Sinaloa in Mexico (Bonin et al., 2006), however, based on

Murphy et al. (2011) these populations are now considered to be G. morafkai. G. agassizii was reported

to have occurred widely over thousands of square kilometres in the Mojave and Colorado deserts until

the middle of the 20th century, with marked declines since (Berry, 1989).

G. agassizii was reported to be found in a wide variety of habitats, including arid canyons, plateaus and

valleys (Bonin et al., 2006) with sandy to rocky substrates (Germano et al., 1994) and scattered shrubs

(U.S. Fish and Wildlife Service, 1994). It has been reported to be found up to an elevation of 2225 m

above sea level (U.S. Fish and Wildlife Service, 2011).

The species is long-lived, with age at reproductive maturity ‘usually assumed to be 15-20 years’ (Turner

and Berry, 1984). A study in 1994 suggested that the mean age at maturity was 14.4 years for populations

in western Mojave and 15.4 years for eastern Mojave populations (Germano, 1994). Campbell et al. (2015)

reported mean annual egg production to be 6.90, with a hatching success of 0.61 and recruitment rates

of between 0.51 and 1.18 females per female per year.

G. agassizii was categorised as Vulnerable by the IUCN, although it was noted in the assessment that it

needed updating (Tortoise and Freshwater Turtle Specialist Group, 1996). Berry (1989) noted that

between 1979 and 1989, populations in most of the 40 plots (>2.6 km2) subject to government agency

monitoring declined by 30-70 per cent over periods of 6 to 10 years. In 2014, population densities of

between 1.5 (El Dorado Valley Tortoise Conservation Area, Eastern Mojave Recovery unit) and 15.3 (Red

Cliff Desert Reserve Tortoise Conservation Area, Upper Virgin River Recovery unit) tortoises per square

kilometre were recorded (U.S. Fish and Wildlife Service, 2015). The same report described population

declines of up to 50 per cent since 2004 in some Tortoise Conservation Areas, with an overall loss of

40 660 adult tortoises since 2004; only one out of five recovery units showed a population increase (U.S.

Fish and Wildlife Service, 2015).

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Gopherus agassizii

Threats to G. agassizii have been reported as disease (Berry et al., 2006), mortality due to traffic

collisions (Boarman and Sazaki, 2006), predation (Kristan and Boarman, 2003; Emblidge et al., 2015),

deliberate injuring and killing of tortoises (U.S. Fish and Wildlife Service, 1994), and habitat loss due to

development (Berry, 1989) and climate change (Barrows, 2011).

Berry (1989) reported that ‘poaching for pets and food’ was a threat to G. agassizii, while collection for

cultural purposes was noted by law enforcement officials (U.S. Fish and Wildlife Service, 1994). Illegal

trade was reported to still be continuing in 2002, however it was noted that there was limited

information to assess the impact of the threat (Boarman, 2002). No evidence for G. agassizii for sale was

found in a survey of 269 online retailers of animals and no exports were reported to the LEMIS database

for the years 1996-2000 (Reed and Gibbons, 2002).

G. agassizii was listed as ‘threatened’ under the Endangered Species Act of 1973, as amended, under

which the collection of listed species from the wild is prohibited (U.S. Fish and Wildlife Service, 1990).

Critical habitat for this species was designated on February 8th 1994 (U.S. Fish and Wildlife Service,

1994). Listing under this act also requires ‘Federal agencies to evaluate their actions with respect to any

species that is proposed or listed as endangered or threatened and with respect to its critical habitat if

any is being designated’ (U.S. Fish and Wildlife Service, 1990). G. agassizii is also protected from

collection under State laws in California, Nevada, Utah and Arizona (U.S. Fish and Wildlife Service,

2010).

G. agassizii populations are the subject of ongoing monitoring, which was initiated by the Bureau of

Land Management (BLM) (U.S. Fish and Wildlife Service, 1994). A recovery plan for the Mojave

population, which was published in 1994 and revised in 2011, requires ‘range-wide, long-term

monitoring’ (U.S. Fish and Wildlife Service & Service, 1994; 2011; 2015). The U.S. Fish and Wildlife

Service and the Utah Division of Wildlife Resources coordinate monitoring at five Recovery Units (U.S.

Fish and Wildlife Service, 2015).

References

Barrows, C.W. 2011. Sensitivity to climate change for two reptiles at the Mojave-Sonoran Desert interface. Journal of Arid Environments, 75(7): 629–635.

Berry, K.H. 1989. Gopherus agassizii Desert Tortoise. In: Swingland, I.R., Klemens, M.W. and Durrell Institute of Conservation and Ecology (Eds.). The Conservation Biology of Tortoises. Occasional Papers of the IUCN Species Survival Commission (SSC) No. 5. Gland, Switzerland.

Berry, K.H., Bailey, T.Y. and Anderson, K.M. 2006. Attributes of desert tortoise populations at the National Training Center, Central Mojave Desert, California, USA. Journal of Arid Environments, 67: 165–191.

Boarman, W.I. 2002. The desert tortoise. In: Boarman, W.I. and Beaman, K. (Eds.). Sensitive animals and plants in the western Mojave Desert. U.S. Geological Survey, Western Ecological Research Center, Sacramento, CA. 1–10.

Boarman, W.I. and Sazaki, M. 2006. A highway’s road-effect zone for desert tortoises (Gopherus agassizii). Journal of Arid Environments, 65(1): 94–101.

Bonin, F., Devaux, B. and Dupré, A. 2006. Turtles of the world. A&C Black, London (UK). 416 pp. Campbell, S.P., Steidl, R.J. and Zylstra, E.R. 2015. Recruitment of desert tortoises (Gopherus agassizii and G.

morafkai: a synthesis of reproduction and first-year survival. Herpetological Conservation and Biology, 10(2): 583–591.

Emblidge, P.G., Nussear, K.E., Esque, T.C., Aiello, C.M. and Walde, A.D. 2015. Severe mortality of a population of threatened Agassiz’s desert tortoises: the American badger as a potential predator. Endangered Species Research, 28: 109–116.

Germano, D.J. 1994. Growth and age at maturity of North American tortoises in relation to regional climates. Canadian Journal of Zoology, 72(5): 918–931.

Germano, D.J., Bury, R.B., Esque, T.C., Fritts, T.H. and Medica, P.A. 1994. Range and Habitats of the Desert

Tortoise. In: Bury, R.B. and Germano, D.J. (Eds.). Biology of North American tortoises. Fish and Wildlife

Research 13. US Department of the Interior, National Biological Survey, Washington D.C. 73–84.

Kristan, W.B. and Boarman, W.I. 2003. Spatial Pattern of Risk of Common Raven Predation on Desert Tortoises.

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Gopherus agassizii

Ecology, 84(9): 2432–2443. Murphy, R.W., Berry, K.H., Edwards, T., Leviton, A.E., Lathrop, A. and Riedle, J.D. 2011. The dazed and confused

identity of Agassiz’s land tortoise, Gopherus agassizii (Testudines, Testudinidae) with the description of a new species, and its consequences for conservation. ZooKeys, 71(113): 39–71.

Reed, R.N. and Gibbons, J.W. 2002. Conservation status of live U.S. nonmarine turtles in domestic and international trade. Available at: http://www.graptemys.com/turtle_trade.doc. [Accessed: 13 September 2016].

Tortoise and Freshwater Turtle Specialist Group 1996. Gopherus agassizii. In: IUCN Red List of Threatened Species. Version 2013.1. Available at: www.redlist.org. [Accessed: 13 September 2016].

Turner, F. and Berry, K. 1984. Population ecology of the desert tortoise at Goffs, California. Available at: http://www.nativefishlab.net/library/textpdf/13432.pdf. [Accessed: 13 September 2016].

U.S. Fish and Wildlife Service 1994. Desert tortoise (Mojave Population) Recovery Plan. Portland, Oregon. 73 pp. U.S. Fish and Wildlife Service 1990. Endangered and threatened wildlife and plants; determination of threatened

status for the Mojave population of the desert tortoise. Federal Register 55:12178-12191. 12178–12191 pp. U.S. Fish and Wildlife Service 2010. Mojave Population of the Desert Tortoise 5-Year Review: Summary and

Evaluation. 123 pp. U.S. Fish and Wildlife Service 2015. Range-Wide Monitoring of the Mojave Population of the Desert Tortoise

(Gopherus agassizii): 2013 and 2014 Annual Reports. Reno, Nevada. 46 pp. U.S. Fish and Wildlife Service 2011. Revised recovery plan for the Mojave population of the desert tortoise (Gopherus

agassizii). Pacific Southwest Region, Sacramento, California. 222 pp.

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Appendix

Table 1: Purpose of trade Code Description

T Commercial

Z Zoo

G Botanical garden

Q Circus or travelling exhibition

S Scientific

H Hunting trophy

P Personal

M Medical (including biomedical research)

E Educational

N Reintroduction or introduction into the wild

B Breeding in captivity or artificial propagation

L Law enforcement / judicial / forensic

Table 2: Source of specimens Code Description

W Specimens taken from the wild

R Ranched specimens: specimens of animals reared in a controlled environment, taken as eggs or juveniles

from the wild, where they would otherwise have had a very low probability of surviving to adulthood

D Appendix-I animals bred in captivity for commercial purposes in operations included in the Secretariat's

Register, in accordance with Resolution Conf. 12.10 (Rev. CoP15), and Appendix-I plants artificially

propagated for commercial purposes, as well as parts and derivatives thereof, exported under the provisions

of Article VII, paragraph 4, of the Convention

A Plants that are artificially propagated in accordance with Resolution Conf. 11.11 (Rev. CoP15), as well as

parts and derivatives thereof, exported under the provisions of Article VII, paragraph 5 (specimens of species

included in Appendix I that have been propagated artificially for non-commercial purposes and specimens of

species included in Appendices II and III)

C Animals bred in captivity in accordance with Resolution Conf. 10.16 (Rev.), as well as parts and derivatives

thereof, exported under the provisions of Article VII, paragraph 5

F Animals born in captivity (F1 or subsequent generations) that do not fulfil the definition of ‘bred in captivity’ in

Resolution Conf. 10.16 (Rev.), as well as parts and derivatives thereof

U Source unknown (must be justified)

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

O Pre-Convention specimens

Appendix