Review of species selected on the basis of the Analysis of ...ec.europa.eu/environment/cites/pdf/reports/Review of species... · Review of species selected on the basis of the Analysis

UNEP-WCMC technical report

Review of species selected

on the basis of the Analysis

of the European Union and

candidate countries’

annual reports to CITES

2012

(Version edited for

1

technical report




candidate countries’


(Version edited for public release)





Review of species selected on the basis of the Analysis of the European Union and candidate countries’

Prepared for The European Commission, Directorate General Environment

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

Published November 2014

Copyright European Commission 2014

Citation UNEP-WCMC. 2014. Review of species selected on the basis of the Analysis of the European Union and

candidate countries’ annual reports to CITES 2012

The UNEP World Conservation M

assessment centre 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

recognize the value of biodiversity and apply this knowledge to all that they

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 designat

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

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

i

Review of species selected on the basis of the Analysis of the European Union and candidate countries’ annual reports to CITES 201

Directorate General Environment, Directorate E - Global & Regional

Global Sustainability, Trade & Multilateral Agreements

Review of species selected on the basis of the Analysis of the European Union and

candidate countries’ annual reports to CITES 2012. UNEP-WCMC, Cambridge.

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

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


ntific research with policy advice and the development of decision tools.

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

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



ses. To ensure that our work is both sustainable and equitable we seek to



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


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


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

UNEP World Conservation Monitoring Centre

environmentally sound

practices globally a

own activities. Printing on

paper from environmentally

sustainable forests and

recycled fibre is

Review of species selected on the basis of the Analysis of the European annual reports to CITES 2012

Global & Regional

Global Sustainability, Trade & Multilateral Agreements, Brussels, Belgium

Review of species selected on the basis of the Analysis of the European Union and

WCMC) is the specialist biodiversity

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


ntific 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

do. To do this, we collate



ses. To ensure that our work is both sustainable and equitable we seek to



ions employed and the presentations do not imply the expressions


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


UNEP promotes

environmentally sound

practices globally and in its

own activities. Printing on

paper from environmentally

sustainable forests and

recycled fibre is encouraged.

ii

Contents

Introduction and summary ............................................................................................................................... 3

Lama guanicoe II/B ........................................................................................................................................... 4

Tridacna maxima II/B ....................................................................................................................................... 8

Euphorbia hedyotoides II/B ............................................................................................................................. 18

Euphorbia itremensis II/B ............................................................................................................................... 20

Euphorbia pedilanthoides II/B ......................................................................................................................... 22

Euphorbia primulifolia II/B............................................................................................................................. 24

Euphorbia sakarahaensis II/B ........................................................................................................................ 28

Elaphe carinata Annex D ................................................................................................................................. 31

Pterapogon kauderni Annex D ....................................................................................................................... 36

Harpagophytum spp. Annex D ...................................................................................................................... 44

Appendix 1 ......................................................................................................................................................... 51

Appendix 2 ........................................................................................................................................................ 53

Introduction and summary

3

Introduction and summary This report presents a review of ten species selected on the basis of the Species selected on the basis of the Analysis of the European Union and candidate countries’ annual reports to CITES 2012.

On the basis of the Analysis of the European Union and candidate countries’ annual report to CITES 2012, 81 taxa were originally selected for review on the basis of noteworthy trends in trade (see Appendix I for methodology).

The 2012 Analysis identified seven Appendix II and Annex B species which may warrant a review on the basis of recent trade levels and taxon status; Lama guanicoe (Chile), Tridacna maxima (French Polynesia) and Euphorbia hedyotoides, E. itremensis, E. pedilanthoides, E. primulifolia, and E. sakarahaensis (Madagascar).

In addition, three Annex D–listed taxa showed noteworthy levels of trade in 2012; Elaphe carinata (China), Pterapogon kauderni (Indonesia) and Harpagophytum spp. (Namibia). It was suggested that these taxa may also warrant further attention.

All ten taxa were selected by the SRG for review. The reviews are presented below.

Lama guanicoe

4

MAMMALIA: CAMELIDAE Lama guanicoe II/B

Taxonomic Note Historically, four subspecies were recognised based on skull measurements, coat colouration, body size

and distribution (Franklin, 2011). Recent molecular studies have identified just two subspecies (González

et al., 2006). Peruvian and northern Chilean populations were reported to be L. guanicoe cacsilensis and

the Bolivian, Argentinian, central and southern Chile were attributed to L. guanicoe guanicoe (Marín et al., 2008; Franklin, 2011).

Trade patterns Lama guanicoe was listed in CITES Appendix II on 12/08/1978 (originally under the synonym Lama glama guanicoe) and in Annex B of the EU Wildlife Trade Regulations on 01/06/1997. Chile has not

published CITES export quotas for this species and has submitted annual reports for all years 2003-2012.

Direct exports of L. guanicoe from Chile to the EU-28 over the period 2003-2012 mainly comprised wild-

sourced meat reported by weight exported for commercial purposes (Table 1). The principal EU importer

was the Netherlands. Smaller quantities of captive-bred specimens for scientific purposes were reported

in trade, predominantly by importers. In addition to the trade presented in Table 1, direct trade to the

EU-28 also included 10 wild-sourced garments (reported by Chile) and 20 leather products (reported by

the importer). Indirect trade to the EU-28 originating in Chile comprised three captive-bred garments

re-exported from Switzerland to France in 2010.

Direct exports to the rest of the world primarily comprised wild-sourced commercially traded skins, the

majority of which were imported by Uruguay (Table 1). Small quantities of scientific specimens were

exported to Argentina in 2007.

COMMON NAMES: Guanaco (English, French, Spanish)

SYNONYMS: Lama glama guanicoe, L. guanicoe cacsilensis, L. guanicoe guanicoe

RANGE STATES: Argentina, Chile, Falkland Islands (Malvinas) (introduced), Paraguay, Peru, Plurinational State of Bolivia

UNDER REVIEW: Chile

EU DECISIONS: Current positive opinion formed on 09/10/2003 for the population of the Gaunaco Conservation and Management Program, Region XII, Magelhanes, Tierra del Fuego, Chile.

Current no opinion formed on 15/03/2005 for specimens from other populations. Previously a 4.6(b) import suspension was in place for Chile from 03/02/2001 to 30/04/2004.

IUCN: Least Concern

Lama guanicoe

5

Table 1: Direct exports of Lama guanicoe from Chile to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. Quantities rounded to one decimal place,

where applicable.

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

EU hair (kg) T C Importer 150 150

Exporter 150 2.5 152.5

W Importer 755 755

Exporter <0.1 0.2 0.2

meat (kg) T W Importer 50405 34028 12400 22000 118833

Exporter 50405.8 44 56400 50000 156849.8

skins T W Importer 75 75

Exporter 20 300 77 397

specimens S C Importer 156 377 2530 3063

Exporter 156 156

W Importer 120 120

Exporter 250 250

RoW skins P W Importer

Exporter 1 1

T W Importer 4 500 504

Exporter 1 104 500 605

specimens S W Importer

Exporter 37 37

Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 14/10/2014

Lama guanicoe

6

Conservation status Lama guanicoe is the one of the largest and most abundant South American ungulates and was reported

to reach 215 cm in height and weigh up to 140 kg (Franklin, 2011). Its native range is large but

discontinuous extending from the Andes of northern Peru to Tierra del Fuego, off the southernmost tip

of South America (Baldi et al., 2008). Current range is less than 40% of the original range (Franklin et al., 1997). The species typically lives in highly seasonal environments including montane habitats up to 4500

m a.s.l., but at higher latitudes it occurs at sea level. Females can breed from the second year and

longevity is 28 years (Franklin, 2011).

Lama guanicoe was considered to be Least Concern due to a wide distribution, presumed large and

stable population, and occurrence of large populations within numerous protected areas (Baldi et al., 2008). The total population was estimated to be 546 000-840 000, with up to 87% thought to occur in

Argentina, where the species is not considered endangered or vulnerable (Franklin, 2011). Baldi et al. (2008) calculated the global population to be under 600 000, however it was stated that population

assessments over a such a wide area should be treated with caution. Franklin (2011) reported that in

Bolivia, the population was small (0.03% of the total) and in Paraguay, the population was considered

very small (0.02% of the total). The population of L. guanicoe cacsilensis remaining in Peru was

estimated to be small and highly fragmented, accounting for 0.62 % of the total, or approximately 3 500

individuals (Franklin, 2011).

Intensification of farming and livestock herding have reduced available habitat and hunting pressure has

impacted many populations (Franklin et al., 1997). Overgrazing has led to degradation of land and

forage quality (Baldi et al., 2012). The species was reported to be hunted for its wool and meat or to free

up forage for sheep (Baldi et al., 2012). In Argentina, more than 220 000 chulengos (juveniles) were

legally killed for their pelts between 1976 and 1979 (Baldi et al., 2012). Entanglement in fences was

reported to be a significant cause of mortality for chulengos; this is caused through enclosure of grazing

land restrict migratory movements of L. guanicoe (Baldi et al., 2012). Interest in the preservation and

conservation of Lama guanicoe has led to development of sustained yield managment of wild

populations in Chile and Argentina (Franklin et al., 1997; Baldi et al., 2012).

In Chile, the species historically ranged over most of the country but the current distribution is

fragmented into separate populations in two distinct regions (Franklin et al., 1997). The southern

populations of L. g. guanicoe occur in the Magallanes and Aysén regions including Tierra del Fuego in

the extreme south (Broad et al., 1988).

The total Chilean population was estimated to be 66 000 individuals (Baldi et al., 2008). Chilean

populations were estimated to account for 12% of the global population (Franklin, 2011). The populations

of the northern subspecies L. guanicoe cacsilensis was reported to be highly endangered and virtually

unknown to science (CONAPA, 2011). The majority of the Chilean population are concentrated in the

southern regions of Magallanes and Aysén (Baldi et al., 2008). Historically, Lama guanicoe (guanicoe)

was most abundant in southern Chile in a landscape dominated by Patagonian steppe, both on the

continental mainland and the island of Tierra del Fuego (Franklin et al., 1997).

A combination of overhunting, human encroachment, fences and competition with domestic livestock

have reduced Lama guanicoe populations throughout its range and in Chile the range was reported to

have been reduced by 75% (Franklin et al., 1997). Remaining populations are confined to fragile

ecosystems with low productivity (Franklin et al., 1997).

Chilean populations have been protected from hunting by law since 1929 (Iriarte, 1986). Additionally,

there are areas in which hunting is prohibited, either with relict populations (7 750 km2), or to protect

Lama guanicoe

7

the species (1 212 km2) (Baldi et al., 2008). However, only 4% of the habitat of L. guanicoe has protection

in eight National Parks and four Reserves, covering an area of 8 354 km2 (Baldi et al., 2008).

References Baldi, B., Lichtenstein, G., González, B., Funes, M., Cuéllar, E., Villalba, L., Hoces, D. and Puig, S. 2008.

Lama guanicoe. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. <www.iucnredlist.org>. [Accessed: 12 September 2014].

Baldi, R., Novaro, A., Funes, M., Walker, S., Ferrando, P., Failla, M. and Carmanchahi, P. 2012. Guanaco management in Patagonian rangelands: a conservation opportunity on the brink of collapse. In: du Toit, J. T., Kock, R. and Deutsch, J. C. (eds.), Wild Rangelands: Conserving Wildlife While Maintaining Livestock in Semi-Arid Ecosystems, Blackwell Publishing, p.266–290.

Broad, S., Luxmoore, R. and Jenkins, M. 1988. Significant trade in wildlife - A review of selected species in CITES Appendix II. Volume 1: Mammals. Gland, Switzerland, Cambridge, UK and Lausanne, Switzerland: IUCN and CITES.

CONOPA, 2011. Instituto de Investigación y Desarrollo de Camilidos Sudamericanos www.conopa.org. [Accessed: 22 October 2014].

Franklin, W. 2011. Family Camelidae (Camels). In: Wilson, D. E. and Mittermeier, R. A. (eds.), Handbook of the Mammals of the World. Volume 2. Hoofed Mammals, Barcelona: Lynx Ediciones, p.206–247.

Franklin, W. L., Fernando, B. M., Bonacic, C. F., Claudio, C. P. and Nicolas, S. V. 1997. Striving to manage Patagonian Guanacos for sustained use in the grazing agroecosystems of southern Chile. Wildlife Society Bulletin, 25 (1), p.65–73.

González, B. O. A., Palma, R. E., Zapata, B. and Marín, J. C. 2006. Taxonomic and biogeographical status of guanaco Lama guanicoe (Artiodactyla, Camelidae). Mammal Review, 36, p.157–178.

Iriarte, J. A. and Jaksic, F. 1986. The fur trade in Chile: an overview of seventy-five years of export data (1910-1984). Biological Conservation, 38, p.243–253.

Marín, J., Spotorno, A., Gonzalez, B., Bonacic, C., Wheeler, J., Casey, C., Bruford, M., Eduardo Palma, R. and Poulin, E. 2008. Mitochondrial DNA variation and systematics of the Guanaco (Lama guanicoe, Artiodactyla: Camelidae). Journal of Mammalogy, 89, p.269–281.

Tridacna maxima

8

MOLLUSCA: TRIDACNIDAE Tridacna maxima II/B

COMMON NAMES: Small giant clam(English)

RANGE STATES: American Samoa, Australia, British Indian Ocean Territory (?), Cambodia,

China, Christmas Island, Cocos (Keeling) Islands, Comoros, Cook Islands,

Egypt, Fiji, French Polynesia, Guam, Hong Kong, SAR (ex), India, Indonesia,

Japan, Kenya, Kiribati, Madagascar, Malaysia, Maldives, Marshall Islands,

Mauritius, Micronesia (Federated States of), Mozambique, Myanmar, New

Caledonia, Niue, Northern Mariana Islands, Palau, Papua New Guinea,

Philippines, Pitcairn Islands, Réunion , Samoa, Saudi Arabia, Seychelles,

Singapore, Solomon Islands, Somalia (?), South Africa, Sri Lanka, Sudan,

Taiwan, Province of China, Thailand, Tokelau, Tonga, Tuvalu, United

Republic of Tanzania, United States of America (?), Vanuatu, Viet Nam,

Wallis and Futuna Islands.

UNDER REVIEW: French Polynesia

EU DECISIONS: Current positive opinion for wild specimens from Australia formed on

22/07/1997 and confirmed on 23/02/2012. Current positive opinion for

French Polynesia formed on 22/07/1997 and last confirmed on 11/09/2012.

Current no opinion (i) for American Samoa, British Indian Ocean Territory,

China, Christmas Island, Cocos (Keeling) Islands, Comoros, Egypt, Guam,

Hong Kong, SAR, India, Indonesia, Kenya, Madagascar, Malaysia, Maldives,

Mauritius, Myanmar, Niue, Northern Mariana Islands, Philippines, Pitcairn

Islands, Samoa, Saudi Arabia, Singapore, Somalia, South Africa, Sri Lanka,

Taiwan (Province of China), Thailand, Tokelau, Tuvalu, United Republic of

Tanzania, United States of America, Wallis and Futuna Islands formed on

02/12/2011, replacing previous positive opinion formed on 22/07/1997.

Current no opinion (i) for Cook Islands, Japan, and Palau formed on

11/09/2012, replacing previous positive opinion formed on 22/07/1997.

Current no opinion (i) for Kiribati formed on 23/02/2012, replacing previous

positive opinion formed on 22/07/1997.

Current no opinion (i) for Papua New Guinea formed on 02/12/2011.

Previous positive opinion for Papua New Guinea formed on 22/07/1997 and

removed on 02/12/2011. Previous no opinion (iii) formed for Papua New

Guinea on 22/05/2003.

Current no opinion (iii) for Seychelles formed on 11/09/2012, replacing

previous positive opinion formed on 22/07/1997 and removed on

11/09/2012.Current no opinion (ii) for Sudan formed on 27/02/2014.

Current Article 4.6(b) import suspension for wild specimens from

Cambodia first applied on 11/07/2013 and last confirmed on 04/09/2014.

Previous negative opinion for Cambodia formed on 11/03/2011 and

Tridacna maxima

9

Taxonomic note Su et al. (2014) separated T. noae, known from Taiwan and Japan, from T. maxima in 2014.

Trade patterns Tridacna maxima was listed in CITES Appendix II on 01/08/1985 as part of the family listing Tridacnidae.

No CITES export quotas have been published for this species from French Polynesia.

French Polynesia is a dependent territory of France and French Polynesia's trade is included in France's

annual reports to CITES. In reports received from France from 2009 onwards, this trade is not

distinguished from trade involving mainland France or other dependent territories. Therefore, from

2009 onwards, it is not possible to distinguish exporter-reported trade from French Polynesia from trade

originating in other dependent territories of France where the species in known to occur (Réunion, New

Caledonia and the Wallis and Futuna Islands). Table 1 below includes all trade from 2003 onwards where

the exporting country was specified as French Polynesia, as well as trade from 2009 onwards where

France was specified as the exporting country (figures for the latter are displayed in brackets).

Direct exports of T. maxima from French Polynesia to the EU principally comprised live, wild-sourced

individuals traded for commercial purposes; the vast majority of this trade was reported in 2011-2012

(Table 1). Smaller quantities of cultures for commercial purposes and shells and specimens for primarily

scientific purposes were also exported.

The vast majority of direct exports from French Polynesia to countries other than the EU also comprised

live, wild-sourced clams for commercial purposes. All trade in live clams was reported in the period

2009-2012, and the United States was the principal trading partner. In addition, the United States

reported the import of 26 live seized/confiscated clams from French Polynesia in 2011.

There were no indirect exports of T. maxima to the EU for which the country of origin was reported as

French Polynesia; however, France reported the import of 100 live, wild-sourced individuals for

commercial purposes in 2012 for which France was also reported as both the origin and re-exporting

country.

confirmed on 07/02/2013.

Current Article 4.6(b) import suspension for wild specimens from Fiji,

Marshall Islands, Federated States of Micronesia, Mozambique, Tonga,

Vanuatu, Viet Nam first applied on 10/05/2006 and last confirmed on

04/09/2014. Previous negative opinion for wild specimens from Fiji,

Marshall Islands, Federated States of Micronesia, Mozambique, New

Caledonia, Tonga, Vanuatu, Viet Nam, formed on 22/05/2003 and

confirmed for Viet Nam on 09/03/2006.

Current Article 4.6(b) import suspension for wild specimens from Solomon

Islands first applied on 10/09/2012 and last confirmed on 04/09/2014.

Previous positive opinion for Solomon Islands formed on 12/03/2009,

replaced with a negative opinion on 12/03/2009 and last confirmed on

02/12/2011.

Current Article 4.6(b) import suspension for wild specimens from New

Caledonia first applied on 30/04/2004 and last confirmed on 04/09/2014.

IUCN: Least Concern

Tridacna maxima

10

Table 1: Direct exports of Tridacna maxima from French Polynesia to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. (Values in brackets represent direct exports of Tridacna maxima from France*. No trade was reported 2005-2007.)

Importer Term Purpos

e Source Reported

by 2003 2004 2008 2009 2010 2011 2012 Total

EU cultures T W Importer (100) (100)

Exporter

live T W Importer 2220

(2900) 2050

(3124) 4270

(6024)

Exporter 3000 (1263) (5870) (8844) 3000

(15977)

shells E W Importer

Exporter 2 2

P W Importer (2) (2)

Exporter 5 5

S W Importer 600 600

Exporter 600 600


Exporter (150) (150)

RoW live T I Importer 26 26

Exporter

W Importer 774 3367 5506 (450) 5126

14773 (450)

Exporter (3318) (8006) (7201) (18525)

Meat (kg) T W Importer

Exporter (2) (2)

shells S W Importer

Exporter 7 7

* These values are included because from 2009 onwards, data reported by France includes exports from mainland France and all dependent territories, including French Polynesia, without distinguishing between these. Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 14/10/2014.

Conservation status Tridacna maxima is a marine mollusc with an important ecosystem role as a food source and substrate

for reef organisms (bin Othman, et al., 2010 and references therein). As with other species in the family

Tridacnidae (giant clams), it was reported to host symbiotic photosynthetic algae in its mantles, and

hence to have a distribution limited to relatively shallow and clear waters (Sutton and Hoegh-Guldberg,

1990; Teitelbaum and Friedman, 2008; bin Othman et al., 2010) to approximately 20 m depth (Kinch and

Teitelbaum, 2010).

The species was reported to reach sexual maturity as males at 3.5 cm length and as hermaphrodites at 2

years of age and 4.5 cm length (Raymakers et al., 2003). Fecundity was found to increase with the age

and size of individuals (Apte et al., 2004); however, high rates of early mortality were reported to lead to

low overall natural recruitment rates (Wells, 1997). Recruitment was reported to be generally stochastic

and unpredictable (Andréfouët et al., 2013). Furthermore, reproduction was found to be unsuccessful at

low densities of mature individuals (Kinch, 2009) and a study in India showed that a minimum density

of 60-100 adults per hectare may be required for successful recruitment (Apte et al., 2004).

T. maxima was considered to be the most widespread species of giant clam (Gilbert et al., 2007), being

widely distributed in the Indo-Pacific region (Andréfouët et al., 2013), and ranging from East Africa to

the Red Sea, eastern Polynesia and Japan (Munro and Heslinga, 1983; Ellis, 1999; bin Othman et al., 2010). The population trend of all Tridacna spp. was considered to be declining in this entire region (bin

Othman et al., 2010). T. maxima was considered to be “reasonably abundant” throughout its range,

although its status in the Indian Ocean was poorly known (Wells, 1997).

Tridacna maxima

11

T. maxima was categorised as Lower Risk/conservation dependent in the IUCN Red List, although the

assessment was noted to require updating (Wells, 1996). The species was considered to be endangered

in many locations worldwide (Gilbert et al., 2006a).

Harvesting pressure of T. maxima was shown to be unsustainable in most areas (bin Othman et al., 2010). Overharvesting for consumption and the souvenir trade was considered to be the main cause of

T. maxima population decline (Apte et al., 2004). The brightly coloured mantle was reported to make

the species particularly attractive for the aquarium trade (Hart et al., 1998; Wabnitz et al., 2003; Kinch

and Teitelbaum, 2008), with higher prices than other Tridacna species (Lindsay et al., 2004). Other

reported threats include predation of juveniles (Chambers, 2007), and potentially, ocean acidification

(Waters, 2008). Mass mortality events have also been reported following fluctuations in sea surface

temperature (Andréfouët et al., 2013; Ronnback et al., 2002).

T. maxima was selected for the CITES Review of Significant Trade process following CoP12

(AC20 Summary Record), with French Polynesia initially included among the 31 countries and territories

selected for review. French Polynesia was then excluded from a more detailed analysis and categorised

as Least Concern, based on an initial analysis of trade data (AC22 Doc. 10.2 Annex 8f; AC22 Summary

Record).

French Polynesia: T. maxima was described as remarkably abundant and dominant in French

Polynesian atolls and island lagoons (Gilbert et al., 2006a). Five atolls in the Tuamoto Archipelago

(Tatakoto, Reao, Fangatau, Napuka, Pukarua) and two islands in the Australes Archipelago (Tubuai,

Raivavae) were reported to have large populations of T. maxima (Andréfouët et al., 2013). While the

species was considered to be abundant in some lagoons and not endangered, it was noted to be depleted

on many islands, particularly the populated Society Islands (Tatarata and Remoissenet, 2009; Gilbert et al., 2006b), Ragiroa in the Tuamotu Islands (Gilbert et al., 2006b) and Tubuai in the Austral Islands

(Larrue, 2006). T. maxima was believed to be the only species of giant clam in French Polynesia until

2006, when T. squamosa was identified in the Astrales archipelago (Gilbert et al., 2007), and a recent

extensive survey revealed the latter species to be rare, but present throughout Tuamotu and Gambier

(Andréfouët and Wynsberge, 2014).

The Fangatau and Tatakoto Atolls were reported to have the highest clam densities observed anywhere

in the world (Gilbert et al., 2006a). Stocks were estimated to be (mean ± 95% confidence interval) 23.6

±5.3 million clams in the 4.05 km2 Fangatau lagoon, 88.3 ± 10.5 million clams in the 11.46 km

2 Tatakoto

lagoon and 47.5 ± 5.2 million clams in the 16.3 km2 Tubuai lagoon (Gilbert et al., 2006a). The biomass

within a 4 km2 survey area of Fangatau Atoll was estimated at approximately 1162 tonnes of meat,

although limiting to commercially available stock above the minimum regulation shell length of 12 cm

gave an estimate of 1038 tonnes (Andréfouët et al., 2005). Similarly, the biomass at Tatakoto and Tubuai

was estimated at 1485 tonnes and 2173 tonnes, with a commercially available stock of 958 tonnes and

1971 tonnes, respectively (Gilbert et al., 2006a). Despite these stock levels, increasing meat harvest for

the market in Tahiti island, combined with mortality events have raised concern over the sustainability

of T. maxima fisheries in the country (Van Wynsberge et al., 2013).

The T. maxima fishery was reported to be developing quickly (Gilbert et al., 2006a). Tubuai Island

(southern French Polynesia) and Tatakoto and Fangatau Atolls were reported to represent nearly the

whole French Polynesian clam market (Gilbert et al., 2006a). In 2004, commercial clam flesh (including

muscle mantle and gonad) exported to Papeete’s market in Tahiti was reported to be 5.5 t for Fangatau,

>16 t for Tatakoto (Gilbert et al., 2006a) and 40 t for Tubuai (Larrue, 2005). In 2002, sales of giant clams

in the Tahiti market were estimated by the Service de la Pêche de Polynésie française (French Polynesia

Fisheries agency, or SPE) to be about 50 t of wet matter per year (Gilbert et al., 2006a).

Tridacna maxima

12

Tridacna maxima was reported to be consumed by French Polynesians for meat, and valued by aquarium

enthusiasts (Andréfouët et al., 2013; Hambrey, 2013). The populations of the Eastern Tuamotu Atolls

were reported to have been harvested for local consumption only until the mid 2000s, when an increase

in exploitation was observed due to rising demand from Tahiti (Andréfouët et al., 2005). The giant clam

population at Takapoto Atoll was reported to have been subject to substantial harvest without sufficient

recruitment, although natural events were reported to be the dominant cause of mortality in this

location (Andréfouët et al., 2005). Fisheries for tourism, including clam tasting, in the Bora Bora lagoon were noted to have impacted T. maxima populations, leading to significant decreases of average shell

sizes of the wild population (Planes et al., 1993). Andréfouët et al.(2009) considered that the rates of

exploitation of T. maxima on Raivavae did not pose a critical threat to the sustainability of the harvest,

but recommended that management should include a system of rotational closures to allow certain

areas to rest.

The Direction des Ressources Marines (DRM) established several measures to control and regulate T. maxima fishing, including a minimum size limit of 12cm for harvest under Decision No. 88-184 AT (1988,

replaced by No. 2002-76 APF) (Commission Permanente, 1988) and monitoring of exports from remote

islands to and through the Tahiti market (Van Wynsberge et al., 2013). The DRM also established

assessments of abundance and population dynamics in several areas (Van Wynsberge et al., 2013). In

addition, the DRM was reported to be establishing No-Take-Areas (NTAs) in several islands, the first of

which came into effect in 2004 in Tatakato (Andréfouët et al., 2013). By 2009, three NTAs and nine

Marine Protected areas had been designated, with 11 and five more planned, respectively (Tatarata and

Remoissenet, 2009). However, spatial modelling of T. maxima in Tubuai and Raivavae led Van

Wynsberge et al. (2013) to conclude that NTAs offered poor efficiency for long-lived, sessile species such

as T. maxima, and may lead to depleted stocks in neighbouring areas due to displacement of fishing

effort. Decreasing catches two-fold using fixed quotas was predicted to increase stock abundance, while

the most efficient indirect management action was predicted to be increasing the minimum shell size

limit (Van Wynsberge et al., 2013). This would allow the clams to reproduce several times before being

fished, though the authors warned that changing a well established size limit may be confusing (Van

Wynsberge et al., 2013). Local restocking was predicted to be insignificant, unless several hundreds of

thousands of clams were reintroduced over several years, which may be possible given the development

of aquaculture, but would require the coordination of “massive efforts” (Van Wynsberge et al., 2013).

The DRM was also reported to be promoting harvest based on cultured giant clams, which could allow

larger exports authorised under CITES, and potentially provide a sustainable supply of giant clam meat

to the Tahiti market, while leaving wild stock undisturbed (Andréfouët et al., 2013), or potentially

restocking (Remoissenet, 2009; in Andréfouët et al., 2013). Tatarata and Remoissenet (2009) reported

that quotas had been established for wild stocks from a restricted selection of lagoons, but that within

three years all exported clams were to be sourced from aquaculture only, with all sizes permitted to be

exported from this source. However, this ambition was not reflected in CITES reported trade, as there

were no reported direct exports in T. maxima from aquaculture in 2003-2012 (Tables 1-2). The failure to

produce meat for export was attributed to several reasons, including: the time taken to produce a

significant flesh yield, production costs, mortality, and the logistics of exporting a fresh product of high

quality (Hambrey, 2013). However, Hambrey (2013) identified that French Polynesia has a significant

opportunity to produce high quality giant clams for the aquarium market through aquaculture,

exporting at least 30 000 clams per year, with clam flesh as a by-product, at least initially, and it is

uncertain whether meat production could be economically viable. Quotas for temporary harvest of wild

stocks for the aquarium trade were set (Andréfouët et al., 2013).

Gilbert et al. (2006, 2006a) reported that massive mortality and patchy mortality events for T. maxima were not uncommon in French Polynesia. These were considered likely to be a result of climatic

Tridacna maxima

13

variation (Andréfouët et al., 2013). In light of mass mortality events, Andréfouët et al. (2013)

recommended:

Replacing the goal of maintaining current stocks for individual islands with a nationwide stock

maintenance objective, so mass mortalities in one location may be balanced with higher

protection elsewhere.

A nationwide network of giant clam spat collecting structures, with a small number dedicated

to the aquarium trade and the others used (in the absence of mortality events) primarily for

meat export and restocking. Where the aquarium trade becomes compromised by mortality

events, other atolls could shift their meat production to the aquarium trade.

Enhanced systematic co-monitoring by communities and scientists to monitor local parameters

relevant to stock levels.

Reported challenges to a new national management plan as described above included: additional costs;

community compliance; and the ability to react to mass mortality events (Andréfouët et al., 2013).

Van Wynsberge et al. (2013) recommended a reduction in total catch until stocks stop decreasing, which

could be implemented by setting quotas until aquaculture operations are developed enough to replace

wild harvests. Larrue (2006) found significant divergence between the views of the scientific community

and the local population on Tubuai with regard to the status of giant clams, which made it difficult to

find a shared approach for the management of the resource. Furthermore, the significant financial

revenues associated with clam fishery were considered to make it difficult to obtain information on local

and national trade, with people being reluctant to disclose information (Larrue, 2006).

The minimum size limit and NTAs were reported to be “virtually unenforced” in Mo’orea (the second

most highly populated island in French Polynesia), with minimal self regulation by fishers and tourism

operators (Yau et al., 2014).

References

Andréfouët, S., Friedman, K., Gilbert, A. and Remoissenet, G. 2009. A comparison of two surveys of invertebrates at Pacific Ocean islands: the giant clam at Raivavae Island, Australes Archipelago, French Polynesia. ICES Journal of Marine Sciences, 66(9): 1825–1836.

Andréfouët, S., Gilbert, A., Yan, L., Remoissenet, G., Payri, C. and Chancerelle, Y. 2005. The remarkable population size of the endangered clam Tridacna maxima assessed in Fangatau Atoll (Eastern Tuamotu, French Polynesia) using in situ and remote sensing data. ICES Journal of Marine Sciences, 62(6): 1037–1048.

Andréfouët, S. and Wynsberge, S. Van 2014. Significance of new records of Tridacna squamosa Lamarck, 1819, in the Tuamotu and Gambier Archipelagos (French Polynesia). Molluscan Research, Advance online publication.

Andréfouët, S., Van Wynsberge, S., Gaertner-Mazouni, N., Menkes, C., Gilbert, A. and Remoissenet, G. 2013. Climate variability and massive mortalities challenge giant clam conservation and management efforts in French Polynesia atolls. Biological Conservation, 160: 190–199.

APF 2007. Assemblée de la Polynésie Française (APF). Déliberation No. 2007-98 du 3 Décembre 2007 relative à la réglementation des activités de collectage, d’élevage et de repeuplement de bénitiers en Polynésie française.

Apte, D., Idrees, B.K.K., Karamathulla, S. and Sutirtha, D. 2004. Species conservation action plan - Ecology, population dynamics and conservation of Giant Clam Tridacna maxima (Roding, 1798) in Lakshadweep Archipelago. Bombay Natural History Society, LEAD International, Darwin Initiative.

Tridacna maxima

14

Chambers, C.N.L. 2007. Pasua (Tridacna maxima) size and abundance in Tongareva Lagoon, Cook Islands. SPC Trochus Information Bulletin, 13: 7–12.

Commission Permanente 1988. Délibération No. 88-184 AT du 8 décembre 1988 relative à la protection de certaines espèces animales marines d’eau douce du patrimoine naturel polynésien.

Conseil des ministres 2008. Arrêté No. 9 CM du 8 janvier 2008 portant application de la délibération n° 2007 - 98 APF du 3 décembre 2007, relative à la réglementation des activités de collectage, d’élevage et de repeuplement de bénitiers en Polynésie française. French Polynesia.

Ellis, S. 1999. Lagoon farming of giant clams (Bivalvia: Tridacnidae). Center for Tropical and Subtropical Aquaculture.

Gilbert, A., Andréfouët, S., Yan, L. and Remoissenet, G. 2006a. The giant clam Tridacna maxima communities of three French Polynesia islands: comparison of their population sizes and structures at early stages of their exploitation. ICES Journal of Marine Science, 63(9): 1573–1589.

Gilbert, A., Planes, S., Andréfouët, S., Friedman, K. and Remoissenet, G. 2007. First observation of the giant clam Tridacna squamosa in French Polynesia: a species range extension. Coral Reefs, 26(2): 229–229.

Gilbert, A., Remoissenet, G., Yan, L. and Andréfouët, S. 2006b. Special traits and promises of the giant clam (Tridacna maxima) in French Polynesia. SPC Fisheries Newsletter, 118: 44–52.

Hambrey, J. 2013. Étude de marché sur l’exportation de bénitiers de culture de Polynésie Française. 26 pp. Hart, A.M., Bell, J.D. and Foyle, T.P. 1998. Growth and survival of the giant clams, Tridacna derasa, T.

maxima and T. crocea, at village farms in the Solomon Islands. Aquaculture, 165: 203–220. Huberman, M. and Eschner, A. 2011. Tridacna (Chametrachea) costata Roa-Quiaoit, Kochzius, Jantzen,

Al-Zibdah and Richter from the Red Sea, a junior synonym of Tridacna squamosina Sturany, 1899 (Bivalvia, Tridacnidae). Annalen Naturhistorisches Museum Wien, 153–162.

Kinch, J. 2009. The importance of giant clam fisheries management and trade to the Pacific. In: Regional management of sustainable fisheries for giant clams (Tridacnidae) and CITES capacity building workshop. CITES, Nadi, Fiji.

Kinch, J. and Teitelbaum, A. 2010. Proceedings of the regional workshop on the management of sustainable fisheries for giant clams (Tridacnidae) and CITES capacity building, 4-7 August 2009, Nadi, Fiji. Noumea, New Caledonia.

Kinch, J. and Teitelbaum, A. 2008. Proceedings of the sub-regional workshop on the marine ornamental trade in the Pacific. SPC (Secretariat of the Pacific Community).

Larrue, S. 2006. Giant clam fishing on the island of Tubuai, Austral Islands group: between local portrayals, economic necessity and ecological realities. SPC Traditional Marine Resource Management and Knowledge Information Bulletin, 19: 3–10.

Larrue, S. 2005. Rapport pour une participation des acteurs socio-économiques à la gestion durable des ressources en bénitiers du lagon de Tubuai. Laboratoire IRIDIP, UPF.

Lindsay, S.R., Ledua, E. and Stanley, J. 2004. Regional assessment of the commercial viability for marine ornamental aquaculture within the Pacific Islands (giant clam, hard and soft coral, finfish, live rock and marine shrimp). Secretariat of the Pacific Community, Aquaculture Section, Noumea, New Caledonia.

Munro, J.L. and Heslinga, G.A. 1983. Prospects for the commercial cultivation of giant clams (Bivalvia: Tridacnidae). In: Proceedings of the thirty-fifth annual Gulf and Caribbean Fisheries Institute. Gulf and Caribbean Fisheries Institute, Marathon, USA. 122–134.

Newman, W.A. and Gomez, E.D. 2000. On the status of giant clams, relics of Tethys ( Mollusca : Bivalvia : Tridacninae ). The Ninth International Coral Reef Symposium, 2: 927-936.

Bin Othman, A.S., Goh, G.H.S. and Todd, P.A. 2010. The distribution and status of giant clams (family Tridacnidae) - a short review. Raffles Bulletin of Zoology, 58(1): 103–111.

Planes, S., Chauvet, C., Baldwin, J., Bonvallot, J., Fontaine-Verneudon, Y., Gabrie, C., Holthus, P., Payri, C. and Galzin, R. 1993. Impact of tourism-related fisheries on Tridacna maxima (Mollusa, Bivalvia) stocks in Bora-Bora lagoon (French Polynesia). National Museum of Natural History, Smithsonian Institution, Washington DC.

Raymakers, C., Ringuet, S., Phoon, N. and Sant, G. 2003. Review of the Exploitation of Tridacnidae in the South Pacific, Indonesia and Vietnam (draft) TRAFFIC, Brussels, Belgium. 75 pp.

Tridacna maxima

15

Remoissenet, G. 2009. French Polynesia case study of giant clam management and trade. Regional Management of sustainable fisheries for giant clams (Tridacnidae) and CITES capacity building workshop. Nadi, Fiji Islands, 4-7 August 2009.

Ronnback, P., Bryceson, I. and Kautsky, N. 2002. Coastal aquaculture development in eastern Africa and the Western Indian Ocean: prospects and problems for food security and local economies. Ambio, 31(7-8): 537–542.

Su, Y., Hung, J., Kubo, H. and Liu, L. 2014. Tridacna noae (Röding, 1798)–a valid giant clam species separated from T. maxima (Röding, 1798) by morphological and genetic data. Raffles Bulletin of Zoology, 62: 124–125.

Sutton, D.C. and Hoegh-Guldberg, O. 1990. Host-zooxanthella interactions in four temperate marine invertebrate symbioses: assessment of effect of host extracts on symbionts. Biological Bulletin, 178(2): 175–186.

Tatarata, M. and Remoissenet, G. 2009. Country presentation French Polynesia. Regional management of sustainable fisheries for giant clams (Tridacnidae) and CITES capacity building workshop. Nadi, Fiji Islands, 4-7 August 2009. 13 pp.

Teitelbaum, A. and Friedman, K. 2008. Current status and prospects for cultured giant clams. SPC. 39 pp.

Wabnitz, C., Taylor, M., Green, E. and Razak, T. 2003. From ocean to aquarium: The global trade in marine ornamental species. UNEP-WCMC, Cambridge, UK. 66 pp.

Waters, C.G. 2008. Biological responses of juvenile Tridacna maxima (Mollusca: Bivalvia) to increased pCO2 and ocean acidification. A thesis submitted in partial fulfillment of the requirements for the degree of Master in Environmental Studies, The Evergreen State College.

Wells, S. 1996. Tridacna maxima. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org. [Accessed: 15/10/2014].

Wells, S.M. 1997. Giant Clams: Status, Trade and Mariculture, and the role of CITES in Management. IUCN, Gland, Switzerland and Cambridge, UK. 77 pp.

Van Wynsberge, S., Andréfouët, S., Gilbert, A., Stein, A. and Remoissenet, G. 2013. Best management strategies for sustainable giant clam fishery in French Polynesia islands: answers from a spatial modeling approach. PloS one, 8(5): e64641.

Yau, A., Lenihan, H. and Kendall, B. 2014. Fishery management priorities vary with self-recruitment in sedentary marine populations. Ecological Applications, 6: 1490–1504.

Euphorbia spp.

16

Overview of Euphorbia spp. in Madagascar

Euphorbia spp. includes over 2,000 species, with representatives distributed throughout the world

(McGough et al., 2004). About 650 species are considered succulent (Oldfield, 1997). Euphorbia species

show a very diverse range of growth forms from annual plants and shrubs to large trees, but are always

characterized by conspicuous milky latex (McGough et al., 2004). Succulent species of the genus

Euphorbia were listed in CITES Appendix II on 01/07/1975, and Annex B of the EU Wildlife Trade

Regulations on 01/06/1997. The current annotation to the listing (#4) states that all parts and derivatives

are listed, except a) seeds, spores and pollen (including pollinia); b) seedling or tissue cultures obtained

in vitro, in solid or liquid media, transported in sterile containers; and c) cut flowers of artificially

propagated plants. Finished products of E. antisyphilitica are also exempt from the listing.

About 60 species of Euphorbia are considered endemic to Madagascar (Dortort, 2011), including the five

species in this review. The biology and ecology of Euphorbia species in Madagascar are poorly known

and research on these species to date has mainly focused on systematics (e.g. Dorsey et al., 2013; Evans et al., 2014; Haevermans et al., 2009).

The main threats to Euphorbia spp. in Madagascar were identified as habitat degradation, fire, habitat

clearing for charcoal, and collection for the horticulture trade (Haevermans, 2004a; 2004b; 2004c;

2004d; 2004g). Coverage by the IUCN Red List of Euphorbia spp. was considered incomplete and

inadequate, with threat levels for many species, especially those in highly restricted natural ranges

thought to be understated or unidentified (PC20 Doc 16.4 Annex 1).

A number of CITES review processes have previously considered Euphorbia spp. from Madagascar. A

review of plant trade from Madagascar was initiated in 2001 (PC 11 Doc. 11.2.1). Following CoP14, fifty-two

Euphorbia spp. were selected as part of the CITES Review of Significant Trade. All succulent Euphorbia species have been subject to the CITES Periodic Review process (Decision 14.131 (Rev. CoP15)). From the

CITES Periodic Review, 199 Euphorbia spp. in Appendix II were identified as at potential risk due to

trade (PC 20. Doc. 16.4 Annex II), however, the PC agreed that no changes to the listing of succulent

Euphorbia spp. included in Appendix II were required (PC 20, Summary Record).

As a result of CITES reviews, an Action Plan for the reform of wildlife trade in Madagascar was initiated

in 2003 (PC 14 Inf. 12). The plan set out actions to improve implementation of CITES including:

addressing national policy and legislation; needs of the CITES Scientific Authority; and management

procedures and enforcement (PC 17 Doc. 8.2). Under this plan field studies for highly traded Euphorbia

spp. were initiated in 2005 and 2006.

Details of the management of Euphorbia spp. within Madagascar were provided for the Review of

Significant Trade in 2010. At that time, there were no specific action plans in place for species of

Euphorbia (CITES Management Authority of Madagascar, Rabesihanaka pers. comm. to UNEP-WCMC,

2010). According to the CITES MA of Madagascar (in litt. to UNEP-WCMC, 2010), Euphorbia spp. could

be harvested from the wild by plant operators which have been approved by the Malagasy State. Harvest

limits were reported to be determined by the Board of Management of the Madagascar CITES Scientific

Authority Flora and the operator. Harvest limits were reported to be based on the species IUCN

category, CITES listing, and the stock status of the species in the wild (CITES MA of Madagascar, in litt. to UNEP-WCMC, 2010).

As a result of Reviews of Significant Trade the CITES MA of Madagascar has been requested to provide

reliable information to establish non-detriment findings for 49 species including 27 Euphorbia species

that were identified as in demand (SC 62 Doc. 27 Rev. 1).

Euphorbia spp.

17

The Scientific Authority conducts an annual inventory of plant stocks to determine the effectiveness of

this artificial increase, basing the annual export quota of each species on the size of available artifically

propagated stocks from operators who had received approval by the Management Authority. This quota

also takes into account the minimal size of specimens suitable for export, with the number of specimens

that can be traded not exceeding 30 per cent of stocks (SC65 Inf. 2). However, the SA cautioned that the

measures would not be fully effective without adequate training of customs officers and border police in

discriminating between wild and artificially propagated specimens (SC65 Inf. 2).

Export quotas for 16 species (including one species included in this review) were set for 2014 (SC 65 Inf.

2). No published details of Madagascan export quotas for other Euphorbia species (for any source) could

be located. Rabesihanaka et al. (2008) also reported that the Madagascan Management and Scientific

Authorities carried out annual visits to plant propagation centres, to check their terms of reference.

Information on this review was requested from CITES MA of Madagascar on 23rd

September 2014 but no

response was received as of 3rd

November 2014.

Madagascar has submitted annual trade reports for CITES listed species for all years 2003-2012.

Euphorbia hedyotoides

18

EUPHORBIALES: EUPHORBIACEAE Euphorbia hedyotoides II/B

Trade patterns

Madagascar has not published export quotas for this species. Direct exports of E. hedyotoides to the EU-

28 during 2003-2012 entirely comprised live plants, the majority of which were traded for commercial

purposes (Table 1). The EU-28 reported 441 live plants imported; France was the principal importer.

Small amounts of trade were reported for personal and artificial propagation purposes. All trade was

wild-sourced with the exception of 300 artificially-propagated plants in 2003 (reported only by

importers) and two artificially-propagated plants reported in 2006 (reported only by Madagascar).

Following the no opinion formed in 2006, there was no trade reported by either party until 2012. No

indirect exports to the EU originating in Madagascar were reported 2003-2012.

Direct exports to countries other than the EU-28 principally comprised live plants for commercial

purposes (Table 1); the main importer was the United States. Trade reported by the exporter decreased

year on year between 2005 and 2009, a similar decrease is seen in importer reported figures.

Table 1: Direct exports of live Euphorbia hedyotoides from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. (No trade reported 2010-2011).

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

EU B W Importer 10 1 11

Exporter

P W Importer

Exporter 21 21

T A Importer 300 300

Exporter 2 2

W Importer 75 55 130

Exporter 92 3 55 150

RoW P A Importer 2 2

Exporter

W Importer

Exporter 2 2

T W Importer 178 119 40 60 55 20 20 492

Exporter 50 119 96 75 60 20 20 440

- W Importer 26 26

Exporter


SYNONYMS: Euphorbia decariana

RANGE STATES: Madagascar

UNDER REVIEW: Madagascar

EU DECISIONS: Current no opinion formed on 12/06/2006, replacing a negative opinion formed on 29/03/2006.

IUCN: Endangered

Euphorbia hedyotoides

19

Conservation status Euphorbia hedyotoides is a dioecious shrub, up to 1.5 m tall with large subterranean bulbs (Rauh, 1992).

It was reported to be endemic to southeastern Madagascar in the Ambovombe/Amboasary area and was

recorded as common throughout its range (Haevermans, 2004a). Rauh (1992) also noted that it was not

rare in the xerophilic Didiereaceae-bush between Amboasary and Taolanaro. It was also recorded from

the Pass of Manangotry (Croizat, 1934). It was reported to have been cultivated as a potential rubber

source in Tanzania early in the last century (Rauh, 1992; Carter and Smith, 1988); however it was noted

to be difficult to cultivate because bulbs die off and propagation by stem cuttings is unreliable (Rauh,

1992).

E. hedyotoides was assessed as Endangered based on the small extent of occurrence (2 594 km²) and a

small area of occupancy (1 100 km²) (Haevermans, 2004a). It has been reported from 15 localities and was

reported to comprise four to five subpopulations (Haevermans, 2004a). E. hedyotoides was reported to

be under threat from habitat degradation, fire, habitat clearing for charcoal, and collection of mature

specimens for the horticultural trade (Haevermans, 2004a). Some localities were reported to fall within

reserves and protected forests (Haevermans, 2004a).

Euphorbia hedyotoides was identified as a priority species for urgent field study. Whilst field studies were planned for 2007 (PC 17 Doc. 8.2) it is not clear if they took place. E. hedyotoides was selected for the Review of Significant Trade following CoP14 and was subsequently removed from the review based on information provided by Madagascar indicating that the species was widespread and not threatened by collection (CoP 15 Doc 7.3.1. (Rev.1)). Under the Periodic Review for Euphorbia spp. initiated under Decision 14.131, (PC19 Doc. 12.3), it was recommended that E. hedyotoides be retained on Appendix II due to the potential risk posed by international trade (PC 19 Doc. 14.2 Rev.1; PC 20 Doc 16.4 Annex 1).

Euphorbia pedilanthoides

20

EUPHORBIALES: EUPHORBIACEAE Euphorbia itremensis II/B

Trade patterns Madagascar has not published any CITES export quotas for this species. Direct exports to the EU-28 primarily comprised live plants of wild origin for commercial purposes (270 as reported by importers), small amounts of wild-sourced trade in personal items were also reported (Table 1). The primary EU importer was Germany. Exports were reported by Madagascar in 2005, 2006 and 2010; EU trading partners also reported exports of 100 plants in 2011 and 2012. No indirect exports to the EU originating in Madagascar were reported 2003-2012.

Direct exports to the rest of the world primarily comprised live wild-sourced plants (Table 1); the United States was the principal importer. The majority of trade was for commercial purposes and trade levels were variable across years, peaking in 2007 (Table X).

Table 1: Direct exports of Euphorbia itremensis from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. No trade was reported 2003-2004.

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

EU dried plants S W Importer

Exporter 1 1

live P A Importer

Exporter 4 4

W Importer

Exporter 21 21

T W Importer 70 100 100 270

Exporter 288 120 100 508

RoW dried plants S W Importer

Exporter 1 1

live P A Importer

Exporter 4 4

W Importer

Exporter 10 10

T W Importer 113 20 220 108 150 80 80 771

Exporter 216 105 290 125 150 210 80 110 1286

- W Importer 45 45

Exporter


Conservation status Euphorbia itremensis is a succulent geophyte, endemic to rocky inselbergs in the high plateau of central

Madagascar between 1 500 - 2 000 m a.s.l. (CITES MA of Madagascar in litt. to UNEP-WCMC, 2013). It



EU DECISIONS: Current no opinion formed on 12/06/2006. Previous negative opinion formed on 29/03/2006

IUCN: Vulnerable


21

was described from specimens collected in 1995 near Itremo (Kimnach and Lavranos, 2001; Haevermans

et al., 2009), and was subsequently recorded from two other sites about 15 km to the south-west

(Missouri Botanical Garden, 2014).

Euphorbia itremensis was categorised as Vulnerable in the IUCN Red List on the basis that it was then only known from one location and, although its area of occupancy and extent of occurrence were unknown, they were likely to be very small (Haevermans, 2004b). Its population trend was also considered to be unknown (Haevermans, 2004b). The main threats to E. itremensis were considered to be habitat degradation, fire, and illegal collection for the horticultural trade (Haevermans, 2004b). It was considered to be one of the five plant species in highest demand in international trade from Madagascar (UNEP/UNCTAD, 2008). Kimnach and Lavranos (2001) found evidence of large-scale uprooting caused by road construction in the type locality of E. itremensis. As part of a review of trade in plants from Madagascar initiated in 2001 (PC 11 Doc 11.2.1), E. itremensis was identified as one of 39 species prioritised for urgent field study in 2005 (PC 17 Doc. 8.2). E. itremensis was selected for the Review of Significant Trade following CITES CoP14 (PC18 Doc. 8.3). The species was later excluded from the review based on a response received from Madagascar confirming that the export of wild-sourced specimens was prohibited (CoP15 Doc. 7.3.1 Rev.1). At PC19, E. itremensis was again included in the Review of Significant Trade as a species of urgent concern (PC19 Summary Record), as wild-sourced specimens had been in trade between 2004 and 2008 (PC19 Doc. 12.4 Annex 1). Further information was sought from Madagascar by the CITES Plants Committee but no data was included in their response (CoP 15 Doc 7.3.1 (Rev.1)). At PC20, the species was retained in the review process based on reported trade in wild-sourced plants and a lack of data on formulation of non-detriment findings (PC20 WG 2 Doc.1).

At PC21, the Plants Committee recommended that the CITES MA of Madagascar should within six

months (i.e. by November 2014): a) inform the secretariat of the methodology for making non-detriment

findings; b) review the available information and data on distribution, conservation, cultivation and

trade status of the species concerned and based on this review and in association with the Secretariat

and the Chair of the Plants Committee, establish a conservative export quota; and c) inform the CITES

Secretariat of this quota, so that it can be included in the national export quotas on the CITES website

(PC 21 WG2 Doc.1).


22

EUPHORBIALES: EUPHORBIACEAE

Euphorbia pedilanthoides II/B

Trade patterns Madagascar has not published export quotas for this species.

Direct exports of E. pedilanthoides from Madagascar entirely comprised live plants and, with the exception of five artificially propagated plants (reported only by Madagascar), all trade was wild-sourced (Table 1). The majority of trade was for commercial purposes, while small amounts of trade were reported for artificial propagation or personal purposes. Fifty live plants were reported by the EU in 2012 by Germany, representing the first instance of trade reported in this species since 2006. No indirect exports to the EU originating in Madagascar were reported 2003-2012.

Direct exports from Madagascar to countries other than the EU-28 solely consisted of live wild-sourced plants, principally for commercial purposes (Table 1). The United States was the main importer of live E. pedilanthoides from Madagascar. No trade has been reported by importers since 2006, whereas Madagascar reported the export of 35 plants in 2007 and 10 plants in 2010.

Table 1: Direct exports of Euphorbia pedilanthoides from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was in live plants. (No trade was reported 2008-2009 and 2011).

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

EU B W Importer 15 10 25

Exporter

P A Importer

Exporter 2 3 5

T W Importer 10 70 53 50 183

Exporter 70 103 173

RoW P W Importer

Exporter 5 5

T W Importer 227 38 110 375

Exporter 38 122 35 10 205

- W Importer 8 12 20

Exporter


Conservation status Euphorbia pedilanthoides is a compact spiny shrub with distinctly thickened base. The flowers are almost totally enclosed by vase-shaped, tubular red bracts (Dortort, 2011). The species was reported to occur in

SYNONYMS: Pedilanthus lycioides



EU DECISIONS: Current positive opinion formed on 02/04/2002.

IUCN: Near Threatened


23

dry sandy forest habitats, which were reported to be highly fragmented (Haevermans, 2004c). E. pedilanthoides was reported to be endemic to western Madagascar in the Ankarafantsika and Morondava areas (Haevermans, 2004c). It was reported to have a large extent of occurrence (44,674 km²) and large area of occupancy (34,234 km²) and was reported from 12 localities, comprising three subpopulations (Haevermans, 2004c). E. pedilanthoides was assessed as Near Threatened in the IUCN Red List (Haevermans, 2004c). However, although the species did not qualify for a threatened category as the time of assessment, it was thought likely that it would continue to be threatened by collection, fires and habitat loss (Haevermans, 2004c). An important protected area for the species was reported to be the Reserve Naturelle Integrale de 1’Ankarafantsika (Oldfield and Supthut, 1997).

E. pedilanthoides was selected for the Review of Significant Trade following CITES CoP14 (PC18 Doc. 8.3).

The species was later excluded from the review based on the response from the Madagascan

Management Authority stating that the species had a large distribution (CoP15 Doc. 7.3.1 Rev.1)). E. pedilanthoides was also excluded from the Periodic Review, as it had been included in the Review of

Significant Trade (PC 19 Doc. 14.2 Rev.1).

Euphorbia primulifolia

24

EUPHORBIALES: EUPHORBIACEAE Euphorbia primulifolia II/B

Taxonomic Note Two variants of the species were delineated by (Cremers, 1984): Euphorbia primulifolia var. primulifolia and Euphorbia primulifolia var. begardii.

Trade patterns Madagascar published a zero export quota in 2013 for E. primulifolia, and an export quota of 533

artificially propagated live plants in 2014.

Direct exports of E. primulifolia from Madagascar to the EU 2003-2012 primarily comprised live wild-

sourced plants (2918 plants as reported by EU importers) (Table 1). The majority were imported for

commercial purposes. Germany was the main EU importer. In addition, small numbers of artificially

propagated plants were reported by importers (two plants in 2003) and the exporter (11 plants in 2005).

Trade for artificial propagation, botanic gardens and as personal items was also reported in small

quantities. Volumes of plants in trade peaked in 2005 at 1180 plants reported by importers and 905

reported by Madagascar. In subsequent years, volumes reported by both importers and exporters were

below 400 live plants.

A negative opinion for wild-sourced specimens was confirmed 29/03/2006 and removed 12/06/2006. No

trade was reported by importers in this year, while Madagascar reported the export of 235 live wild-

sourced exports to the EU-28. A second negative opinion for wild-sourced E. primulifolia was formed on

09/09/2012, confirmed on 07/12/2012 and replaced with a no opinion iii) on 28/05/2014. Trade in 2012

comprised 350 plants reported by importers and 20 plants reported by exporters. In both cases the

negative opinion only applied to part of the year. No indirect exports to the EU originating in

Madagascar were reported 2003-2012.

Direct exports to countries other than the EU principally comprised commercial exports of live wild-

sourced plants (Table 1). A small number of artificially propagated plants were reported in 2005 (12

reported by importers, three reported by the exporter) and small quantities of plants were also traded as

personal items. The United States was the principal importer of live E. primulifolia from Madagascar.

SYNONYMS: Euphorbia primulifolia var. primulifolia, Euphorbia primulifolia var. begardii



EU DECISIONS: Current no opinion (iii) formed on 28/05/2014.

Previous negative opinion formed on 03/09/2012 (confirmed 07/12/2012).

A negative opinion was formed on 29/03/2006. This was removed and replaced with a no opinion (iii) on 12/06/2006.

IUCN: Vulnerable


25

Table 1: Direct exports of Euphorbia primulifolia from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012.

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

EU live B W Importer 155 75 230

Exporter

G A Importer 2 2

Exporter

W Importer 12 12

Exporter

P A Importer

Exporter 11 11

W Importer 15 15

Exporter 12 31 43

T W Importer 630 1165 216 300 350 2661

Exporter 200 863 235 300 2 20 1620


Exporter 1 1

RoW live P A Importer 12 12

Exporter 3 3

W Importer 25 14 39

Exporter 5 12 14 10 41

T W Importer 2625 80 25 243 63 300 270 185 340 4131

Exporter 200 157 151 478 478 300 410 185 340 2699

- W Importer 5 74 79

Exporter


Exporter 2 2 Source: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 14/10/2014

Conservation status Euphorbia primulifolia var. primulifolia is a geophyte with large, fleshy tubers up to several kilos in

weight, remaining mostly underground and producing an annual rosette of 4-6 lanceolate leaves, 8-11 cm

in length (Cremers, 1984). The leaves die off after flowering and fruiting, and the plant then lies dormant

until the next rainy season (Rauh, 1995). It produces branched stems each with 2-4 pairs of pale green

flowers about 1 cm across shortly before new leaves appear (Cremers, 1984; Dortort, 2011).

The habitat was reported to include coastal sands in northeastern Madagascar, whereas inland it was

reported from relatively cool places in the central highlands including: rocky limestone woods, basaltic

lawns and quartzite and gneiss rockeries (Evans et al., 2014; Cremers, 1984). Euphorbia primulifolia var.

primulifolia was reported to be the more widespread variant, and was considered common throughout

its range (Haevermans, 2004f). It was reported to have a small extent of occurrence (7671 km2) and a

small area of occupancy (3481 km2) (Haevermans, 2004f).

Cremers (1984) mapped the distribution of E. primulifolia var. primulifolia along the central plateau from

northeastern Madagascar to the Sakaraha area in the south west. E. primulifolia var. begardi was

reported to be limited to the vicinity of Isalo in the southwest. It was reported from 15 locations and four

subpopulations (Haevermans, 2004f). Localities reported by (Cremers, 1984) for the primulifolia variant

were: Majunga and environs; Manongarivo (Ambongo); plateau of Ankara; Antanimena plateau between

Mahavavy and Betsiboka; Firinglava between Maevetanana and Andriba; edge of Bemarivo; Antanimena

(Boina); Beronono dunes on the Maha Jamba (Boina); Antsirabe; Mount Tritivo; 22-23 km, road


26

Arivonimano; between Ambatomainty and Itremo; mountains W of Itremo; Plateau Horombe; Soalala

R.N.; Betafo Decary; near Tananarive Decary. Euphorbia primulifolia type location was reported to be

Ankaratra mountains (Haevermans et al., 2009).

E. primulifolia var. begardii is a more branched variant and was reported from coarse sands around Isalo

(Cremers, 1984). It was reported to be common throughout its range but to have a very small extent of

occurrence (317 km2) and area of occupancy (66.5 km

2) in valleys around Isalo in southwest Madagascar

(Haevermans, 2004e). It was reported from coarse sands in four localities and to comprise three to four

subpopulations (Haevermans, 2004e). More recently, the Madagascar SA for flora (2014) reported E.

primulifolia var. begardii to have a fragmented distribution over 9491 km2 in the south-east, with an area

of occupancy of 32 km2, representing 6 sub-populations, one of them inside protected areas, and a

predicted future decline of 83%.

Both variants of this species are considered threatened due to habitat degradation, limited extent of

occurrence and the small number of populations (Haevermans, 2004d). The major threats were reported

to be habitat degradation, fire, and collection for horticulture (Haevermans, 2004d). Some localities fall

within reserves and protected forests such as Parc National d’Isalo (Haevermans, 2004d; Oldfield and

Supthut, 1997), however Oldfield and Supthut ( 1997) suggested that the area needed to be extended to

include land south of National Route No.7 and north of the Onilahy River. The area was reported to be

regularly visited by succulent plant collectors (Oldfield and Supthut, 1997). Healthy adult plants were

reported to be collected for export, resulting in severe impacts on the regeneration of the species

(Madagascar SA for flora, 2014).

The Madagascar SA for flora (2014) reported densities of both varieties of 1000 individuals per ha in sites

surveyed, but noted that their regeneration rates were low (61% for primulifolia and 23% for begardii).

E. primulifolia var. primulifolia and E. primulifolia var. begardii were selected for the Review of

Significant Trade following CITES CoP14 (PC18 Doc. 8.3). The Plants Committee subsequently decided

not to review varieties separately (PC 18 Summary Record). At CoP15 (2010), the Plants Committee chair

reported that Madagascar had provided information on the population in Madagascar, indicating that

the species was widespread in its habitat and not threatened by collection (CoP15 Doc. 7.3.1 Rev.1),

however the species was retained in the review process. Euphorbia primulifolia was subsequently

categorised as of Urgent Concern (PC 19 Summary Record) due to the high volume of trade in a globally

threatened species (PC 19 Doc. 12.4). For species of Urgent Concern, Madagascar was required, within

three months, to establish a voluntary export quota system, put in place a zero export quota for wild

specimens, and to inform the Secretariat of the process under which the non-detriment finding was

made before reopening trade (PC19 Summary Record).

In December 2012, Madagascar reported that the export quota was voluntarily set to zero for 27 species

of Euphorbia including E. primulifolia, pending obtaining reliable information to establish non-

detriment finding (PC 21 Doc. 21.1). In 2014, the CITES Scientific Authority of Madagascar reported that

the export of wild specimens of certain Euphorbia species (including E. primulifolia) was prohibited

(SC65 Inf. 2). The Madagascar SA (2014) for flora recommended a trade ban for at least five years.

It was reported that operators had been authorised to collect, on a one-off basis, wild specimens to

supply parent plants for their nurseries (SC65 Inf. 2). In 2014, the actual stock of artificially propagated

E. primulifolia was reported to be 1778 individuals, with an authorised export quota of 533 individuals


27

(SC65 Inf. 2). This quota will be updated annually following inspections of operators and analysis of the

number of specimens in trade (SC65 Inf. 2).

Euphorbia sakarahaensis

28

EUPHORBIALES: EUPHORBIACEAE Euphorbia sakarahaensis II/B

Trade patterns Madagascar has not published export quotas for E. sakarahaensis. Direct exports of E. sakarahaensis to the EU-28 comprised entirely of wild sourced live plants for commercial purposes (128 live plants, as reported by EU importers), (Table 1). Germany was the principal EU importer. Madagascar reported exports in 2005 and 2006; in addition to this trade, importers reported trade in 2004 (five live plants) and 2012 (50 live plants); trade reported by importers in 2012 was the first instance of trade recorded in this species since 2006. No indirect exports were reported to the EU in 2003-2012.

Direct exports to countries other than the EU consisted of live wild-sourced plants, the vast majority of which was for commercial purposes (Table 1). The United States was the principal trading partner, reporting the import of 200 live plants over the 10 year period; Madagascar reported this quantity as 100.

Table 1: Direct exports of Euphorbia sakarahaensis from Madagascar to the EU-28 (EU) and the rest of the world (RoW), 2003-2012. All trade was in live plants. (No trade was reported in 2003, 2008-2009 and 2011).

Importer Purpose Source Reported by 2004 2005 2006 2007 2010 2012 Total

EU T W Importer 5 70 3 50 128

Exporter 70 3 73

RoW P W Importer 4 4

Exporter 4 4

T W Importer 155 50 5 210

Exporter 100 15 20 10 145

- W Importer 10 10

Exporter


Conservation status Euphorbia sakarahaensis is a shrub with tuberous roots (Evans et al., 2014). It is reported to grow under trees in dry forest habitats (Haevermans, 2004g). It is known only from the Sakaraha (Zombitsy) area, from where it was described in 1991 although the exact distributional range is not known (Haevermans, 2004g; Haevermans et al., 2009). Evans et al., (2014) noted that there were four localities in their sources but no further details were provided. The main threats to the species were reported to be habitat degradation, fire, habitat clearing for charcoal, and collection for the horticulture trade (Haevermans, 2004g; PC 18 Doc. 16.1.2). Some locations were reported to fall within reserves and protected forests (Haevermans, 2004g). As part of the review of trade in plants from Madagascar initiated in 2001 (PC 11 Doc 11.2.1) E. sakarahaensis was identified as one of 39 species prioritised for urgent field study in 2005 (PC 17 Doc.



EU DECISIONS: -

IUCN: Vulnerable


29

8.2), however is not clear if these studies took place. The species was also selected for the Review of Significant Trade following CoP14. Responding to a request for information on status of the species from the CITES secretariat in 2008, the CITES MA of Madagascar confirmed that an export ban was in place and only artificially propagated plants were exported (PC 18 Summary Record). The species was consequently excluded from the Review of Significant Trade (PC 18 Summary Record).

References Carter, S. and Smith, A. 1988. Euphorbiacaea (Part 2). In: Polhill, R. M. (ed.), Flora of Tropical East

Africa, Rotterdam: A.A. Balkema. 602 pp. CITES Management Authority of Madagascar. 2010. Rabesihanaka, S. pers. comm. to UNEP-WCMC, 07-

09-2010. CITES Management Authority of Madagascar. 2013. CITES Management Authority of Madagascar, in litt. to UNEP-WCMC, 14/03/2013. Cremers, G. 1984. Les euphorbes géophytes de Madagascar. Bulletin du Jardin Botanique National de

Belgique, 54 (3-4), p.367–391. Croizat, L. 1934. Three new Euphorbia from Madagascar. The National Horticultural Magazine, 98, p.96-

99. Dorsey, B. L., Haevermans, T., Aubriot, X., Morawetz, J. J., Riina, R., Steinmann, V. W. and Berry, P. E.

2013. Phylogenetics, morphological evolution, and classification of Euphorbia subgenus Euphorbia. Taxon, 62 (2), p.291–315.

Dortort, F. 2011. The Timber Press guide to succulent plants of the world: a comprehensive reference to more than 2000 species. Portland, Oregon: The Timber Press. 344 pp.

Evans, M., Aubriot, X., Hearn, D., Lanciaux, M., Lavergne, S., Cruaud, C., Lawry II, P. and Haevermans, T. 2014. Insights on the evolution of plant succulence from a remarkable radiation in Madagascar (Euphorbia). Systematic biology, 63 (5), p.697–711.

Haevermans, T. 2004a. Euphorbia hedyotoides. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: <www.iucnredlist.org> [Accessed: 23 September 2014].

Haevermans, T. 2004b. Euphorbia itremensis. IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. Available at: www.iucnredlist.org [Accessed: 28 May 2013].

Haevermans, T. 2004c. Euphorbia pedilanthoides. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org [Accessed: 24 September 2014].

Haevermans, T. 2004d. Euphorbia primulifolia. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org [Accessed: 24 September 2014].

Haevermans, T. 2004e. Euphorbia primulifolia var. begardi. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org [Accessed: 2 October 2014].

Haevermans, T. 2004f. Euphorbia primulifolia var. primulifolia. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org [Accessed: 2 October 2014].

Haevermans, T. 2004g. Euphorbia sakarahaensis. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.2. Available at: www.iucnredlist.org [Accessed: 24 September 2014].

Haevermans, T., Rouhan, G., Hetterscheid, W., Teissier, M., Belarbi, K., Aubriotand, X. and Labat, J.-N. 2009. Chaos revisited: nomenclature and typification of the Malagasy endemic Euphorbia subgenus Lacanthis (Raf .) M. G. Gilbert. Adansonia, 31 (2), p.279–299.

Kimnach, M. and Lavranos, J. 2001. A new Madagascan Euphorbia: E. itremensis. Cactus and Succulent Journal, 73 (1), p.42–47.

McGough, H. N., Groves, M., Mustard, M., Brodie, C. and Sajeva, M. 2004. CITES and Succulents. An introduction to succulent plants covered by the Convention on International Trade in Endangered Species. Kew. 200 pp.

Missouri Botanical Garden 2014 http://www.tropicos.org Accessed 06/11/2014. Oldfield, S. 1997. Status survey and conservation action plan: Cactus and succulent plants. Gland,

Switzerland and Cambridge, UK: IUCN/SSC Cactus and Succulent Specialist Group. 226 pp. Oldfield, S. and Supthut, D. 1997. Madagascar. In: Oldfield, S. (ed.), Status survey and conservation

action plan: Cactus and succulent plants, Gland, Switzerland and Cambridge, UK: IUCN/SSC Cactus and Succulent Specialist Group, p.59–67.


30

Rabesihanaka, S. S., Rakouth, B., Ravavaripalala, A., Rarivoson, T. I., Rabouth, H., Ravaomanalina, H., Rabotondrazaby, A., Rabesoa, R. and Rabesihanaka. 2008. National Wildlife Trade Policy Review. Madagascar. UNEP-UNCTAD CBTF, CITES & IUED, p.1–80.

Rauh, W. 1992. The growth-form of Euphorbia hedyotoides N. E. Br. (syn. E. decariana Croiz.). Collectanea Botanica, 21, p.191–195.

Rauh, W. 1995. Succulent and xerophytic plants of Madagascar. Vol. 1. Mill Valley, California: Strawberry Press, p.343.

Ujwala, K. and Karpagam, N. 2013. Potential therapeutical values of plant latices. International Journal of Medicinal and Aromatic Plants, 3 (2), p.317–325.

UNEP-WCMC 2014. EU wildlife trade 2012: Analysis of the European Union and candidate countries’ annual reports to CITES 2012. UNEP-WCMC, Cambridge.

UNEP/UNCTAD. 2008. National Wildlife Trade Policy Review: Madagascar. Geneva, Switzerland: United Nations Environment Programme and United Nations Conference on Trade and Development.

Elaphe carinata

31

REPTILIA: COLUBRIDAE Elaphe carinata Annex D

Trade patterns Elaphe carinata was listed on Annex D of the EU Wildlife Trade Regulations on 01/06/1997. The

listing applies to live specimens, whole or substantially whole dead specimens, and any whole, or

substantially whole skins (raw or tanned).

Direct exports to the EU-28 principally comprised skins, the majority of which were reported

without a purpose or source code (Table 1). Small quantities of skins were reported for

commercial purposes, this trade was either wild-sourced or reported as source unknown. Direct

imports of skins increased year on year from 25 635 in 2009 to over 122 000 in 2012. The primary

EU importer was Italy. Notable quantities of small leather products were also directly imported to

the EU; the vast majority of which were reported without purpose or source codes. The majority

of this trade was reported in 2003 (23076 items) and since 2008 quantities have remained below

100 items per year. Direct imports of plates reported in number were first recorded in 2008, and

trade levels have increased year on year from 89 to 7673 in 2012.

In addition to the above trade, there were also direct imports of this species from Hong Kong,

SAR to the EU-28 (Table 2). Italy was the main EU importer. This trade primarily comprised small

leather products reported without a purpose or source code, while notable quantities of skins and

skin pieces were also reported, again without source or purpose code. No records of occurrence of

the species in Hong Kong could be located.

Indirect exports to the EU originating in China principally comprised skins exported via Hong

Kong SAR to Italy. This trade was reported 2009-2011 and was reported without a purpose or

source code (Table 3). Notable quantities of wild-sourced small leather products were re-exported

to Spain via Hong Kong for commercial purposes in 2005 and 2006.

This species is not included in the CITES Appendices; no export quotas have been published by

China.

COMMON NAMES: Taiwan stink snake (English); Élaphe carénée (French)

RANGE STATES: China, Japan, Taiwan, Province of China, Viet Nam

UNDER REVIEW: China

EU DECISIONS: none

IUCN: Not assessed

Elaphe carinata

32

Table 1: Direct exports of Elaphe carinata from China to the EU-28, 2003-2012.

Term Unit Purpose Source 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 Total

leather products (large) - - - 280 25 305

leather products (small) - T W 2 2

- 43 43

- - 23076 5123 120 432 14 61 14 28840

live - T U 27 27

W 50 10 52 5 117

- - 29 29

plates m2 - - 126 944 1070

- - - 89 173 259 5377 7673 13571

skins - T U 160 160

W 2221 2221

- - 8925 25635 92811 93069 122449 342889


Table 2: Direct exports of Elaphe carinata from Hong Kong, SAR to the EU-28 (EU), 2003-2012. (No trade was reported 2006-2007 and 2009).

Term Purpose Source 2003 2004 2005 2008 2010 2011 2012 Total

leather products (small) - 3500 2541 6041

live T W 60 60

plates - 55 10 65

skins - 1488 70 68 100 1726

skin pieces - 2040 2040


Table 3: Indirect exports of Elaphe carinata originating in China to the EU-28, 2003-2012.

Term Purpose Source 2005 2006 2007 2009 2010 2011 2012 Total

leather products (small) T W 11952 1392 49 13393

- - 64 64

plates - - 24 4 236 264

skins - - 257 15755 6843 22855


Elaphe carinata

33

Taxonomic note: Guo et al. (2012) stated that three subspecies had been described; E. c. yonaguniensis (endemic to

Ryukyu islands, Japan and Taiwan), E. c. carinata and E. c . deqinensis. Based on morphological

characters, Guo et al. (2012) synonymised E. c. deqenensis with E. c. carinata. Smith et al. (1995)

recognised E. c. yonaguniensis and E. c. deqinensis and also E. c. orithophaga.

Conservation status Elaphe carinata is a large predatory constrictor of up to 2m in length, which inhabits plains, hills and

mountains (Zhou and Jiang 2004). It is distributed within Eastern Asia, including China and Taiwan,

north Viet Nam, and the Ryukyu Archipelago in Japan (Wallach et al. 2014).

Wallach et al. (2014) recorded the species distribution from southern and eastern China, including:

Anhui, Beijing, Fujian, S. Gansu, Guangdong, Guangxi, Guizhou, Henan, Hubei, Hunan, Jiangsu, Jiangxi,

Shaanxi, Shandong, Sichuan, Tianjin, Yunnan, Zhejiang, Lanyu Is. It was also reported from Shanghai,

Hainan and Taiwan, Province of China, by Zhou and Jiang (2004). Chen (2009) considered E. carinata as

an indicator species for the southwest region of China.

The species was classified as Vulnerable according to the China Red Data Book of Endangered Animals

(Zhao, 1998 in: Zhou and Jiang, 2004). Population surveys in Zhejiang province found densities of 4.57

individuals/km2, with the species found in downhill and valley areas, in plains, farmland and shrubby

habitats (Tao et al. 2003). Xianlin et al. (1998) considered that data on “resources and domestic

utilization” were not available for E. carinata, but referred to a “preliminary statistical” inventory

number of the main distribution area at the beginning of the 1990’s of 7 555 229 or about 5 341 548 kg.

Zhou and Jiang (2004) reported that international trade was “significant” for E. carinata; and that the

species was in the top four species exported from China as skins (39% of exports overall), with 2 460 767

skins exported during 1990-2001, in addition to 110 113 individual live snakes exported over the same

period. Export data reported by Xianlin et al. (1998) suggests that average trade in E. carinata was

around 290 000 skins between 1990 and 1996, and that trade levels may have declined over this period

(Table 4).

Table 4. Exports of Elaphe carinata, according to Xianlin et al. (1998). No data presented for 1989 and 1993.

Year Live Skin (piece)

1988 150 6000

1990 16621 520008

1991 32250 531870

1992 18640 363000

1994 4440 94700

1995 1750 80500

1996 2000 165650

The Humane Society of the United States (2001) reported that Elaphe carinata was the fifth most highly

imported reptile to the United States in 1997, with 37 412 live individuals imported from China in that

year, although it was noted that some of this trade may have comprised skins rather than live animals. E. carinata was also reported to be consumed locally in China (Wang et al. 2011); many snake species are

also used for traditional medicines (Jiang et al. 2013).

According to Jiang et al. (2013), consumption of snakes in China was banned in 2004, and their use in

traditional medicines was regulated in 2007. No specific protection or management measures for E. carinata could be located. However, the species was reported to occur in a number of protected areas in

China. In a rapid biodiversity assessment, E. carinata (shed skin) was found in forest of the Huaping

Elaphe carinata

34

National Nature Reserve in northeast Guangxi (South China) in 1998 (Kadoorie Farm and Botanic

Garden, 2002a). It was also recorded from the Mulun National Nature Reserve, North Guangxi (Zhou,

1995 cited in Kadoorie Farm and Botanic Garden, 2002b), and from the Nanling National Nature

Reserve, northwest Guangdong (Li, 1996 cited in Kadoorie Farm and Botanic Garden, 2003a). E. carinata

was also reported from the Chebaling National Nature Reserve, northeast Guangdong (Liang, 1993, cited

in Kadoorie Farm and Botanic Garden, 2003b) and from the Jiulianshan Nature Reserve, South Jiangxi

(Dai, 2002 cited in Kadoorie Farm and Botanic Garden, 2003c). It was also recorded from the Wuyishan

Nature Reserve in Fujian province (a World Heritage Area and Biosphere Reserve) (Wu and Cai, 1994

and Wang Sung 1999, cited in Boyd et al. 2003); snake collection was reported to occur in this protected

area (Boyd et al. 2003).

Xianlin et al. (1998) discussed how export quotas for E. carinata in China could be based on yearly

export data, however it is unclear if quotas have been set, or their basis. Zhou and Jiang (2004)

recommeded that national surveys for E. carinata were required in order to establish scientifically based

catch and export quotas.

References

Chen, Y. 2009. Conservation biogeography of the snake family Colubridae of China. North-Western Journal of Zoology, 5(2): 251-262.

Dai, N.H. 2002. Checklist of reptiles from Jiulianshan Nature Reserve. In: Liu, X.Z., Xiao, Z.Y. and Ma, J.H. (eds.) Scientific Survey and Study on the Forest Ecosystem in Jiangxi Jiulianshan Nature Reserve. China Forestry Publishing House, Beijing. 448 pp. (In Chinese.) 251-253.

Guo, P., Liu, Q., Myers, E. A., Liu, S., Xu, Y., Liu, Y., & Wang, Y. 2012. Evaluation of the validity of the ratsnake subspecies Elaphe carinata deqenensis (Serpent : Colubridae). Asian Herpetological Research, 3(3): 219–226.

Jiang, Z., Zhou, Z., Meng, Z., Meng, X., Li, L., Ping, X., Zeng, Y, and Mallon, D.P. 2013. Domestic and CITES regulations controlling the international snake trade in China. Oryx, 47(04): 532–534.

Kadoorie Farm and Botanic Garden. 2002a.Report of a rapid biodiversity assessment at Huaping National Nature Reserve, northeast Guangxi, China, 15 to 20 August 1998. South China Forest Biodiversity Survey Report Series (Online Simplified Version) No. 15. Hong Kong, SAR. 22 pp.

Kadoorie Farm and Botanic Garden. 2002b. Report of a rapid biodiversity assessment at Mulun National Nature Reserve, North Guangxi, China, 18 to 23 July 1998. South China Forest Biodiversity Survey Report Series (Online Simplified Version) No. 13. Hong Kong, SAR. 26 pp.

Kadoorie Farm and Botanic Garden. 2003a. Report of a rapid biodiversity assessment at Nanling National Nature Reserve, Northwest Guangdong, China, June-July 2000. South China Forest Biodiversity Survey Report Series No. 29. Hong Kong, SAR. 33pp.

Kadoorie Farm and Botanic Garden. 2003b. Report of rapid biodiversity assessments at Chebaling National Nature Reserve, Northeast Guangdong, China, 1999, 2000 and 2001. South China Forest Biodiversity Survey Report Series No. 32. Hong Kong, SAR. 26pp.

Kadoorie Farm and Botanic Garden. 2003c. Report of rapid biodiversity assessments at Jiulianshan Nature Reserve, South Jiangxi, China, 2000, 2001 and 2003. South China Forest Biodiversity Survey Report Series No. 33. Hong Kong, SAR. 21pp.

Li, Z.C., 1996. Herpetofauna of Dadongshan Nature Reserve with description of two new records in Guangdong. Journal of South China Normal University (Natural Science), 1996(2): 80-83.

Liang, Q., 1993. The reptilian fauna in National Chebaling Nature Reserve (preliminary report). Pp. 257-261. In: Xu, Y. (ed.), Collected papers for investigation in National Chebaling Nature Reserve. Guangdong Science and Technology Press, Guangdong, 553 pp. (In Chinese with English abstract.)

Smith, H., Ota, H. and Wallach, V., 1995. Phyllophis carinata Gunther, 1864 (currently Elaphe carinata; Reptilia, Serpentes); proposed conservation of the specific name. Bulletin of Zoological Nomenclature, 52(2): 166–169.

Elaphe carinata

35

Tao, J., Liu, A., Yang, Y., Sun, M. and Weng, W. 2003. Research on population quantity and ecological distribution of main snakes in Zhejiang Province. Journal of Zhejiang University (Agriculture and Life Science), 29(5): 563–568.

Wallach, V., Williams, K.L. and Boundy, J., 2014. Snakes of the world: a catalogue of living and extinct species CRC press. 1257 pp.

Wang, F., Zhou, L., Gong, S., Deng, Y., Zou, J., Wu, J., Liu, W. and Hou, F. 2011. Severe infection of wild-caught snakes with Spirometra erinaceieuropaei from food markets in Guangzhou, China involves a risk for zoonotic sparganosis. The Journal of parasitology, 97(1): 170–1.

Xianlin, M., Jianzhang, M., Huapeng, C., Hong, C., Erhu, G. and Zhanqiang, W. 1998. Wildlife export quota and its administrative system. Journal of Forestry Research, 9(2): 95–101.

Zhou, F., 1995. Vertebrate resources. In Zheng, Y.W. (ed.), Scientific Reports of the MulunKarst Forest. Unpublished report, 235 pp. (In Chinese.) 138-155.

Zhou, Z. and Jiang, Z., 2004. International trade status and crisis for snake species in China. Conservation Biology, 18(5): 1386–1394.

Pterapogon kauderni

36

ACTINOPTERYGII: APOGONIDAE Pterapogon kauderni Annex D

CITES history A proposal to include P. kauderni in CITES Appendix II under Criterion B of Annex 2a of Resolution

Conf. 9.24 (Rev. CoP13), was submitted to CoP14 (2007) by the United States of America (CITES CoP14

Prop 19 and CoP14 Inf. 37). Indonesia, as the only range State, did not support the proposal, stating their

committment to sustainable management and highlighting the importance of local livelihoods (CoP14

Com. 1 Rep. 10 (Rev. 1)). The FAO Ad Hoc Expert Advisory Panel did not support the proposal,

concluding that P. kauderni did not meet the biological critera for Appendix II listing, nor did the

proposal demonstrate a decline to criterion levels for population size (no evidence of decline in area of

occurrence or number of subpopulation levels to criterion levels) (FAO, 2007). FAO (2007) also noted

concern that an Appendix II listing may hinder national management of the species. The proposal was

withdrawn by the United States.

Trade patterns Pterapogon kauderni was listed on Annex D of the EU Wildlife Trade Regulations on 11/4/2008.

Direct exports to the EU from Indonesia primarily comprised live individuals (Table 1). The majority of

this trade was reported without a purpose or source code, and is assumed to be of wild origin. The

purpose of trade was either commercial or unreported. Direct exports to the EU from Indonesia

exceeded 10 000 individuals in all years 2009-2013 except for 2011; direct exports of live fish (reported by

number) in 2013 represented the highest volumes in trade in this period (15 988). In addition, over 2000

kg of live fish was reported in 2013. The main importers were the United Kingdom and Germany. No

indirect exports of P. kauderni to the EU originating in Indonesia were reported 2008-2013.

Table 1: Direct exports of Pteropogon kauderni from Indonesia to the EU-28 (EU) 2008-2013.

Term Unit Purpose Source 2008 2009 2010 2011 2012 2013 Total

derivatives - - - 97 28 125

live - T C 60 60

U 744 1561 4795 6885 6139 20124

W 77 77

- 1010 1010

- I 86 6 92

- 10217 11226 439 7034 9849 38765

COMMON NAMES: Banggai cardinalfish; Metallic cardinalfish

RANGE STATES: Indonesia

UNDER REVIEW: Indonesia

EU DECISIONS: none

IUCN: Endangered

Pterapogon kauderni

37

Term Unit Purpose Source 2008 2009 2010 2011 2012 2013 Total

kg - - 2178.4 2178.4

Sources: CITES Trade Database, UNEP-WCMC, Cambridge, UK, downloaded on 14/10/2014; Annual reports for UK and Belgium for 2013.

Pterapogon kauderni trade data reported within the United States Law Enforcement Management

Information System (LEMIS) database was requested from the U.S Fish and Wildlife Service. Whilst data

within LEMIS indicated that only 70 live specimens were imported to the U.S during 2007-2014, this was

acknowledged to be a substantial underestimate of actual trade levels because many shipments are

reported simply as “live tropical fish” (CITES Management Authority of the United States of America,

pers. comm. to UNEP-WCMC, 2014). The species was reported as “frequently imported into the United

States for the aquarium trade” (CITES Management Authority of the US, pers. comm. to UNEP-WCMC,

2014). Using shipment declarations and commercial invoices for live marine tropical fish submitted to

the U.S Fish and Wildlife Service, Rhyne et al. (2012) reported that P. kauderni was among the top 10

marine aquarium fish imported to the U.S during May 2004-May 2005. Based on the data presented by

Rhyne et al. (2012), U.S imports over this period appeared to be in the region of 180,000 fish.

Conservation status Pterapogon kauderni is a small marine fish endemic to the Banggai Archipelago in the eastern part of

Central Sulawesi, Eastern Indonesia (Allen and Donaldson, 2007). It occurs in shallow (<6m), sheltered

waters, most commonly between 1.5-2.5m depth, in reef habitats, seagrass beds, and open areas of sand

and rubble, predominately on the protected side of larger islands (Allen and Donaldson, 2007).

However, it can occur in environments with a strong surge and moderate currents (Vagelli and

Erdmann, 2002). The species is site-attached, remaining close to hiding substrates (branching corals, sea

urchins), maximally 1m from ocean floor (Allen, 2000; Vagelli and Erdmann, 2002; Bernardi and Vagelli,

2004). Kolm and Bergland (2003) found P. kauderni densities to be positively correlated with sea urchin

densities. Whilst all ages were found in Diadema urchin habitat, sea anemones were considered

especially important as a microhabitat type for newly released recruits and juveniles (Moore et al., 2012;

Ndobe et al., 2013a).

P. kauderni has the lowest recorded fecundity of any apogonid, with clutch sizes of approximately 50

eggs (Vagelli and Erdmann, 2002). Sexual maturity was thought to be reached at one year, with species

longevity of 3-5 years (Ndobe et al., 2013b). Reproductive biology is unusal; there is a high degree of

parental care; males brood the egg clutch for 20 days and the hatched eggs for a further 10 days in the

oral cavity (Bernardi and Vagelli, 2004; Vagelli and Volpedo, 2004).

A lack of a pelagic larval phase results in limited dispersal capability and localised settlement and

recruitment (Allen, 2000; Allen and Donaldson, 2007; Bernardi and Vagelli, 2004). Life history traits

combined with oceanographic conditions of the Banggai region (deep channels and strong currents

separting islands) were considered to have contributed to limited gene flow (Bernardi and Vagelli,

2004). These characteristics mean that P. kauderni is unable to recolonise in areas from which it has

been extirpated (Vagelli, 2008; Ndobe and Moore, 2013).

A high degree of genetic variation between isolated populations seperated by only a few km was

reported by Hoffman et al. (2005). Twelve distinct populations were found around the island of

Bangkulu, which is only 60km in perimeter (Vagelli et al., 2009). Five seperate stocks were also reported

from Banggai Island based on morphometric methods (Ndobe and Moore, 2013).

The restricted range of the species covers an area of around 5,500km2, but with maximim potential

habitat of only around 34km2 (Vagelli, 2005, in: CoP14 Prop 19). Extent of distribution covers 74 sites in

30 islands; P. kauderni occurs in 17 of the 20 major islands and 10 of the 27 minor islands within the

species natural distribution in the Banggai Archipelago (Allen and Donaldson, 2007). Several

Pterapogon kauderni

38

subpopulations inhabiting large islands were considered isolated, including those on the east coast of

Tempaus, Masoni Island, south Bokan, Bangkulu Island, Masoni Island and Labobo (Allen and

Donaldson, 2007). Populations on all other large islands are separated by no more than 5km from

another large island subpopulation (Allen and Donaldson, 2007).

Introduced populations occur at four sites in the Lembeh Straight in North Sulawesi around 400 km

north of range, in the Lewuk habour in Central Sulawesi (Erdmann and Vagelli, 2001; Allen and

Donaldson, 2007), in Mamboro in Pulu Bay, on the opposite site of Sulawesi, 440 km west of the Banggai

Archipelago (Moore and Ndobe, 2007), and in north Bali (Lilley, 2008). An introduced population was

recently discovered in Kendari, in southeast Sulawesi (Moore et al., 2011).

P. kauderni is categorised as Endangered in the IUCN Red List on the basis of a very small area of

occupancy, severe fragmentation, a continuing population decline and local extirpations due to

exploitation for trade (Allen and Donaldson, 2007).

In a rapid assessment of the Banggai Islands in 1998, P. kauderni was found to be locally common in

sheltered habitats (Allen and McKenna, 2001). Vagelli and Erdmann (2002) surveyed three sites (Bokan,

Limbo and Masoni) in 2001, observing average densities of 0.03 individuals/m2, based on 4,000 animals

in 92 groups. Extrapolating over the species range, population size was estimated to be in the region of

1.7 million fish (Vagelli, 2002 in: Allen and Donaldson, 2007). Following additional surveys in 2002 and

2004 over the entire Archipelago (50 islands, 159 sites), the population was estimated at approximately

2.4 million individuals by using average densities of 0.07 indiv/km and estimated available habitat

(Vagelli, 2005 in: CoP14 Prop 19). The largest population was estimated to be at Peleng (619,360

individuals), with the populations of Banggai island, Bangkulu island and Taliabu island all estimated to

be greater than 200,000 (Vagelli, 2005 in: CoP14 Prop 19).

Negative effects on populations were first observed in 2000, five years after the export fishery opened

(Kolm and Berglund, 2003). Dramatic declines as a result of fishing pressures were observed between

2001 and 2004, including complete extinction of a the Limbo Island subpopulation in 2004, which

according to a 2001 census was around 50,000 individuals (density of 0.02 fish/m2) in 2001 (Allen and

Donaldson, 2007). A small subpopulation of 6,000 individuals off Bakakan Island in 2001 was reduced to

17 individuals in 2004 (Vagelli, 2005; in Allen and Donaldson, 2007; CoP14 Prop 19). Vagelli (2008)

reported the population of Masoni to be reduced to only 37 individuals in 2007, and the population of

Peleng to be practically eliminated, with only 27 individuals surveyed.

The United States considered that strong biological indications pointed to population declines,

including declines in densities, CPUE, mean group size and maximum number of fish per group; it was

thought probable that fishing pressure had extirpated subpopulations from specific areas (CoP14 Inf. 37).

Between 2000 and 2004, weekly catches were reported to have declined by 25%-80% (1000 fish/hour to

25-300 fish/hour) off North Banggai (CoP14 Inf 43).

P. kauderni density in the only protected bay closed to fishing within the species distribution was found

to be 0.63 individuals/m2 (Allen and Donaldson, 2007); almost 10 x higher than average densities in non-

protected sites found throughout the Archipelago. Whilst the FAO (2007) considered that direct

comparison of these densities was invalid; the United States disagreed (CoP14 Inf. 37).

Site assessments undertaken by Marine Aquarium Council Indonesia in 2007 at Luwuk, Banggai, Bone

Baru, Bone Bone, Liang, and Teropot also showed that population sizes were smaller at recent collection

sites; it was also reported there was general agreement from collectors that the populations were

suffering from overexploitation, with sites being abandoned following collapse (Lilley, 2008).

Pterapogon kauderni

39

Yahya et al. (2012) surveyed 54 sites from 2007-2012 using a 100 m x 5 m belt transect method, with site

selection based on previous P. kauderni surveys and information from local communities and fishermen.

The species was recorded as present in 28 of the 54 areas surveyed, with the species being most common

around Banggai Island and smaller islands to the south of range, and mostly absent from Pelang Island,

northwest of Banggai Island (Yahya et al., 2012). Three sites were surveyed in both June 2009 and July

2012 (Teropot, Bone Baruth, and Popisi) and at these sites changes in population structure were noted

(declines in adults and recruits and but increases in juveniles) leading to overall population declines

(Yahya et al., 2012).

The main threat to P. kauderni was considered by Allen and Donaldson (2007) to be heavy collection for

the aquarium trade. Fisheries were reported from all of the major islands within the species range (Lunn

and Moreau, 2004) with most of the trade reported to be destined for the United States, Europe and Asia

(Kolm and Berglund, 2003; CoP14 Prop. 19 ). In 2001, 50,000-60,000 individuals per month were received

for export from North Sulawesi, with additional exports from Bali (Vagelli and Erdmann, 2002). Lunn

and Moreau (2004) estimated that 118,000 fish were sold monthly from Tumbak and Palu in 2001.

Harvest and trade was estimated at 700,000-900,000 fish/yr for 2001-2004 (CoP14 Prop. 19). For the

period 2004-2006, estimates of trade were 600,000-700,000 fish/year (Moore et al., 2012). Vagelli (2008)

estimated capture levels at that time to be around 1 million specimens per year.

Since 2006, the scale of the fishery was reported to have been reduced; P. kauderni fishing grounds had

reportedly been reduced from 12 villages in 2001, to just three in 2011 (Moore et al., 2012). These were

Bone Baru and Tolokibit (Banggai island), and Bone Bone (Bangkurung island)(Moore et al., 2011; Moore

et al., 2012). Catch data from the Banggai Cardinalfish Centre (BCFC) for 2008 indicated that catches

from two sites totalled 236,373 individuals (162,940 from Bone Baru, 73,433 from Toropot; no data for

Bone Bone) (Moore et al., 2012). Combined catch data for all three sites for 2009 was 330,416 (Moore et al., 2012). Legal shipments of P. kauderni for 2009 and 2010 as reported by the BCFC were 215,950 and

148,800, respectively (Moore et al., 2011; Moore et al., 2012). Whilst these figures were not considered a

complete trade record; they were thought to show a reduction in overall trade volumes (Moore et al., 2011). Yahya (2012) reported that in 2010 and 2011, 99,898 and 99,719 individuals respectively were

shipped from Bone Baru to other major Indonesian cities for distribution.

International demand for P. kauderni was estimated by the Marine Aquarium Council and Indonesian

Nature Foundation (LINI) in 2008 to be approximately 450,000 fish/year (Moore et al., 2011; Moore et al., 2012). The gap between supply and estimated demand in earlier years was considered by Moore et al. (2012) to be due to high levels of mortality and rejects (damaged fish), in addition to speculative buying

practise, which led to release of unsold fish and several introduced populations along trade routes.

Other threats to P. kauderni habitat were reported to be increasing, in particular the intensive

harvesting of shallow water invertebrates for consumption locally, including Diadema urchins (often

used to feed carnivorous reef fish such as Cheilinus undulatus for illegal export) and sea anemones,

which are important microhabitat species (Moore et al., 2012; Ndobe et al., 2013a). Habitat loss and

harvesting of sea urchins and anemones was reported to result in a loss of refuges for recruits and

increase vulnerability of P. kauderni to predation (Yahya, 2012).

The P. kauderni population of Tinakin Laut suffered a drastic decline following disappearance of sea

anemones which had been consumed during a drought period; similar declines were observed at

Mamboro in Palu Bay (Moore et al., 2012). Community-based population monitoring revealed reduced

densities of P. kauderni at sites with low fishing pressure; these declines were attributed to the harvest of

ecologically important urchin and anemones (Moore and Ndobe, 2013). Collection methods of pushing

sea urchins into a cage which the fish then follow was also considered to impact on urchin populations

(Kolm and Berglund, 2003).

Pterapogon kauderni

40

Further anthropogenic threats to P. kauderni were reported to include habitat destruction caused by

destructive fishing practises (explosives, cyanide, coral destruction through netting fish) (Allen, 2000;

Allen and McKenna, 2001; Moore et al., 2012) and coastal development, effluent discharge, and terrestrial

water run-off (Lilley, 2008; Moore et al., 2012; Yahya, 2012). However, the species was reported to be

quite tolerant of pollution, occurring at some highly impacted sites such as Luwak and Banggai harbours

(Vagelli and Erdmann, 2002). Coral mining and predation by Acanthaster plancii were also reported

(Ndobe et al., 2013a). Coral reef degradation was noted at several sites in the Banggai Archipelago during

surveys in 2004 and 2006 (Moore and Ndobe, 2009), and coral cover had declined in P. kauderni habitat

in Bone Baru from 2004 to 2011 (Moore et al., 2012).

P. kauderni is not a protected species in Indonesia under Government Regulation No. 7/1999 (President

of the Republic of Indonesia, 1999). Thornhill (2012) reported that authority for management of marine

resources in Indonesia was designated to regional governments. Management actions for P. kauderni were reported to include a multi-year Banggai Cardinalfish Action Plan (2007-2012), developed by local

and national stakeholders (Ndobe and Moore, 2009); inclusion of the species conservation within the

Indonesian National Coral Triangle Initiative plan; and a district Marine Protected Area (MPA)

including 10 islands with conservation of P. kauderni as the primary aim at Banggai and Togong Lantang

islands (Ndobe et al., 2012).

Actions of the the Banggai Cardinalfish Action Plan included obtaining baseline survey data and

monitoring of the population, conservation awareness campaigns, fisheries management plans,

initaition of MPAs, research, capacity building and regulation of the trade (Ndobe and Moore, 2008).

Implementation of the plan was reported to include the establishment of the Banggai Cardinfish Centre

(BCFC) in Banggai town to act as a central point from which management decisions and efforts could be

coordinated with local communities (Lilley, 2008; Moore and Ndobe 2013). However, it was reported

that the BCFC had no operational budget and activities had been carried out on a voluntary basis, or

with limited support (Moore et al., 2011).

According to Moore and Ndobe (2013) further actions that had been implemented included the drafting

of legislation in the form of a BCF Fisheries Management Plan and village legislation for coastal resource

management, the establishment of a district protected area network in 2007, and habitat

conservation/restoration activities at community level. Additional activities had reportedly included

training for fishermen on sustainable harvest methods and post-harvest handling; development of more

efficient and equitable trading, and catching fish to order, made possible as a result of more direct air

transport routes (Moore et al., 2012; Moore and Ndobe, 2013). A trade monitoring system at the three

main trading centres was reported to have been implemented in 2008 and run in partnership with local

stakeholders and the Marine and Fisheries Research Agency (BRKP) (Moore and Ndobe, 2013).

Local fisherment were reportedly active in conservation in Bone Baru, including the establishment of a

community MPA and protecting the species from destructive fishing and havesting of invertebrates

(Moore et al., 2012; Moore and Ndobe, 2013). Populations at two of the main collection sites (Bone Baru

and Teropot) which had experienced declines from 2007, were reported to have increased again in 2012;

it was suggested this could be attributed to the closure of collection sites at Bone Baru in 2010 and

Bongo Beach in 2012 by local community groups (Yahya et al., 2012). Decreases in illegal trade,

destructive fishing practise (especially collection of brroding males) and mortality were all reported

(Moore et al., 2011).

Reksodihardjo and Lilley (2007, in: Lilley 2008) considered that meetings involving national and local

stakeholders, government, NGOs and traders had helped to create a coordinated approach to

management, but Lilley (2008) reported that community development in Banggai including no-take

zones had been piecemeal and not integrated into the Banggai Marine Conservation Area Management

Pterapogon kauderni

41

Plan. Ndobe et al. (2012) noted overall improvements to the management of the fishery since 2007, but

considered that threats to habitat and microhabitat loss remained unaddressed, as did Yayha (2012).

Lilley (2008) noted the lack of no-take zones as part of a coordinated regional plan; and problems with

nearshore no-take zones set up by villagers destroyed by people from elsewhere. The requirement for

non-local collectors to obtain harvest permits in order to harvest the species was not considered to be

enforced (Thornhill 2012). Moore et al. (2011) reported that whilst irregular monitoring had been carried

out by several individuals and organisations, no comprehensive monitoring system had been

implemented and few types of data were being collected on a regular, long-term basis.

Specific activities were outlined in Indonesia’s National Plan of Action for the Coral Triangle Initiative

for P. kauderni; these included a species action plan and population assessments, development of a trade

database and certification scheme, trade monitoring and enforcement and capacity building (National

Secretariat of CTI-CFF Indonesia, 2009). In 2011, implementation had not yet started (Jompa, 2009, pers.

comm to Moore et al., 2011).

In relation to the district MPA, it was reported that three included islands which had P. kauderni populations were not specifically designated for protection of the species; whilst the species was actually

absent from one site (Togong Lantang) which had been designated with specific protection for P. kauderni (Ndobe et al., 2012). The MPA was considered to have been poorly designed from conservation

perspective in terms of maintaining the intraspecific genetic diversity of P. kauderni; 15 of the 17 distinct

genetic stocks were reported to remain outside of MPA boundaries (Ndobe et al., 2012).

Illegal and unreported fishing were reported to continue, although efforts to curb these activities were

noted to be in place (Moore et al., 2012). Control and enforcement of management measures were still

considered to be lacking in the field (Yahya, 2012). Harvest and export was reported to be occurring

without being reported, and measures to monitor control and control trade were not considered

effectively enforced by Yayha (2012). Trade quotas proposed by local stakeholders in 2010 were

reportedly not continued because of lack of legal support (Yayha, 2012).

Whilst P. kauderni was considered as on the way towards sustsainble fishery (Moore et al., 2011), several

authors noted the lack of resources (e.g. manpower, coordination, skills and funding) were weakening

the capacity for protection of the species (Lilley, 2008, Moore et al., 2011, Thornhill, 2012).

Captive breeding of the species was reported to be a viable alternative to wild harvest (CoP14 Prop 19). P. kauderni was considered to be hardy in captivity and could be bred in captive conditions for commercial

purposes (Roozbehfar et al., 2012). Ongoing research programmes as part of the Banggai Cardinalfish

Action Plan were reported to exist at aquaculture research agencies in Ambon and Bali (Moore and

Ndobe, 2013).

References Allen, G., 2000. Threatened fishes of the world: Pterapogon kauderni Koumans, 1933 (Apogonidae).

Environmental Biology of Fishes, 57, p.142. Allen, G. and Donaldson, T., 2007. Pterapogon kauderni. In: IUCN 2007. 2007 IUCN Red List of

Threatened Species. ver 2014.2 Allen, G.R. and McKenna, S.A., 2001. A marine rapid assessment of the Togean and Banggai Islands,

Sulawesi, Indonesia. In RAP Bulletin of Biological Assessment No. 20. Washington D.C., USA: Conservation International. 145 pp.

Bernardi, G. and Vagelli, A., 2004. Population structure in Banggai cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Marine Biology, 145(4): 803–810.

CITES Management Authority of the United States of America, 2014. Mark Albert pers. comm. to UNEP-WCMC, 15/10/2014.

Erdmann, M. V and Vagelli, A., 2001. Banggai cardinalfish invade Lembeh Strait. Coral Reef, 20: 252–253.

Pterapogon kauderni

42

FAO, 2007. FAO Fisheries Report No. 833 Report of the second FAO ad hoc expert advisory panel for the assessment of proposals to amend Appendices I and II of CITES concerning commercially-exploited aquatic species, Rome. 134 pp.

Hoffman, E.A., Kolm, N., Berglund, A., Arguello and J.R., Jones, A.G. 2005. Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Molecular Ecology, 14(5): 1367–75.

Kolm, N. and Berglund, A., 2003. Wild populations of a reef fish suffer from the “nondestructive” aquarium trade fishery. Conservation Biology, 17(3): 910–914.

Lilley, R., 2008. The Banggai cardinalfish: An overview of conservation challenges. SPC Live Reef Fish Information Bulletin, 18: 3–12.

Lunn, K.E. and Moreau, M. -a., 2004. Unmonitored trade in marine ornamental fishes: the case of Indonesia’s Banggai cardinalfish (Pterapogon kauderni). Coral Reefs, 23(3): 344–351.

Moore, A. and Ndobe, S., 2007. Discovery of an introduced Banggai Cardinalfish population in Palu Bay, Central Sulawesi, Indonesia. Coral Reefs, 26(3): 569–569.

Moore, A., Ndobe, S., Salanggon, A. and Rahman, A. 2012. Banggai cardinalfish ornamental fishery: The importance of microhabitat. Proceedings of the 12th International Coral Reef Symposium, (July): 9–13.

Moore, A. and Ndobe, S., 2009. Reefs at risk in Central Sulawesi, Indonesia - status and outlook. Proceedings of the 11th International Coral Reef Symposium, Ft.Lauderdale, Florida, 7-11 July, 1(840-844).

Moore, A. and Ndobe, S., 2013. The Banggai cardinalfish: An overview of management and conservation initiatives. Galaxea, Journal of Coral Reef Studies, (Special Issue): 238–242.

Moore, A., Ndobe, S. and Zamrud, M., 2011. Monitoring the Banggai cardinalfish , an endangered restricted range endemic species. Journal of Indonesia Coral Reefs, 1(2): 99–113.

National Secretariat of CTI-CFF Indonesia, 2009. Indonesia National Plans of Action, 52 pp. Ndobe, S., Setyohadi, D., Herawati, E.Y., Soemarno and Moore, A. 2012. An ecological and social

approach to Banggai cardinalfish conservation management. In Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia, 9-13 July 2012. Cairns: 9–13.

Ndobe, S., Moore, A., Madinawati, N. and Serdiati, N. 2013a. The Banggai cardinalfish: An overview of local research (2007 - 2009 ). Galaxea, Journal of Coral Reef Studies: 243–252.

Ndobe, S., Herawati, E.Y., Setyohadi, D., Moore, A., Palomares, M.L.D. and Pauly, D. 2013b. Life history of Banggai cardinalfish, Pterapogon kauderni (Actinopterygii: Perciformes: Apogonidae), from Banggai Islands and Palu Bay, Sulawesi, Indonesia. Acta Ichthyologica Et Piscatoria, 43(3): 237–250.

Ndobe, S. and Moore, A., 2013. Banggai cardinalfish (Pterapogon kauderni) populations (stocks) around Banggai Island, a geometric and classical morphometric approach. PeerJ PrePrints.

Ndobe, S. and Moore, A., 2008. Banggai cardinalfish: towards a sustainable ornamental fishery. In Proceedings of the 11th International Coral Reef Symposium, Ft.Lauderdale, Florida, 7-11 July. Florida: 1026–1029.

President of the Republic of Indonesia, 1999. Nomor 7 Tahun 1999 Tentang Pengawetan Jenis Tumbuhan Dan Satwa. Peraturan Pemerintah Republik Indonesia.

Reksodihardjo, G.L and Lilley, R., 2007. A community-based action plan fior the management of the Banggai cardinalfish. OFI Journal 55: 23-25.

Rhyne, A.L., Tlusty, M.F., Schofield, P.J., Kaufman, L., Morris, J.A. and Bruckner, A.W., 2012. Revealing the appetite of the marine aquarium fish trade: the volume and biodiversity of fish imported into the United States. PloS one, 7(5): e35808.

Roozbehfar, R., Mehdi, B., Kiani, F. and Sedaghat, M. 2012. Captive breeding of Banggai cardinalfish, Pterapogon kauderni (Koumans, 1933) for exit of IUCN Red List. World Journal of Zoology, 7(4): 273–278.

Thornhill, D.J., 2012. Ecological impacts and practices of the coral reef wildlife trade, Washington D.C., USA: Defenders of Wildlife.

Vagelli, A., 2002. Notes on the biology, geographic distribution, and conservation status of the Banggai cardinalfish Pterapogon kauderni Koumans 1933, with comments on captive breeding techniques. Tropical Fish Hobbyist: 84–88.

Vagelli, A., Burford, M. and Bernardi, G., 2009. Fine scale dispersal in Banggai Cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Marine genomics, 1(3-4): 129–34.

Pterapogon kauderni

43

Vagelli, A.A., 2005. Reproductive biology, geographic distribution and ecology of the Banggai cardinalfish Pterapogon kauderni Koumans, 1933 (Perciformes, Apogonidae), with Considerations on the Conservation Status of this Species on its Natural Habitat.,

Vagelli, A.A., 2008. The unfortunate journey of Pterapogon kauderni: A remarkable apogonid endangered by the international ornamental fish trade, and its case in CITES. SPC Live Reef Fish Information Bulletin, 18: 17–28.

Vagelli, A.A. and Volpedo, A. V, 2004. Reproductive ecology of Pterapogon kauderni, an endemic apogonid from Indonesia with direct development. Environmental Biology of Fishes, 70: 235–245.

Vagelli, A.R. and Erdmann, M., 2002. First comprehensive ecological survey of the Banggai cardinalfish, Pterapogon kauderni. Environmental Biology of Fishes, 63(1).

Yahya, Y., Mustain, A., Artiawan, N., Reksodihardjo-Lilley, G. and Tlusty, M.F. 2012. Summary of results of population density surveys of the Banggai cardinalfish in the Banggai Archipelago, Sulawesi, Indonesia, from 2007-2012. AACL Bioflux, 5(5): 303–308.

Harpagophytum spp.

44

SCROPHULARIALES: PEDALIACEAE Harpagophytum spp. Annex D

CITES history Germany proposed the listing of H. procumbens and H. zeyheri in Appendix II at CoP11 (Prop

11.60); the latter species for lookalike reasons. The proposal outlined localised population

depletions and increasing international trade. Range States were consulted on the proposal.

According to Setshogo (2013), Range States noted that it was not based on substantiated and

quantified data, there was insufficient evidence of the threatened status of the species, and it was

considered that an Appendix II listing would impact on livelihoods of poor and marginalised

communities. Germany’s proposal failed to gain support from Range States and was withdrawn,

although Decision 11.63 directed the Range and importing states to submit all available

information concerning the trade, management and biological status of Harpagophytum spp., and

the regulatory measures applying to them to the Secretariat.

Trade patterns The genus Harpagophytum was listed in Annex D of the EU Wildlife Trade Regulations on

20/05/2004. As an Annex D species, trade data is only available from EU-28 importer-reported

data.

Direct exports to the EU-28 from Namibia over the period 2003-2012 comprised trade reported as

H. procumbens and trade reported at the genus level Harpagophytum spp. as reported by the EU-

28 only. The principal term in trade was roots reported by weight, and the majority of trade was

reported as wild-sourced for commercial purposes, although notable quantities were reported in

2008 and 2012 without a purpose or source code specified (Table 1). In total, roughly 773 000 kg

(all terms combined) was recorded at the genus level, with the remaining trade recorded at the

species level. Direct imports of Harpagophytum roots from Namibia increased by more than 6-

fold between 2011 and 2012, primarily due to an increase in reported imports by Germany and

Poland, although Italy and Spain also reported imports in 2012. Germany was the main EU

importer of Harpagophytum spp. over the period.

Indirect exports to the EU-28 originating in Namibia solely comprised 14 500 kg of live plants

exported to France via an unknown exporting country in 2011. No source or purpose was reported

for this trade.

COMMON NAMES: Devil’s claw, Grapple plant

RANGE STATES: Angola, Botswana, Mozambique, Namibia, South Africa, Zambia, Zimbabwe

UNDER REVIEW: Namibia

EU DECISIONS: none

IUCN: Not assessed

Harpagophytum spp.

45

Table 1: Direct exports of Harpagophytum from Namibia, 2005-2012. All trade was imported by the EU-28 only.

Term (Unit) Purpose Source 2005 2006 2007 2008 2009 2010 2011 2012 Total

dried plants (kg) T W 28788.8 10290.6 17492 62303 21200 13933.6 154008

leaves (kg) T W 9216 9216

medicine (kg) - - 57000 24.9 57024.9

powder (kg) T W 6004.5 6004.5

roots (kg) T W 51060 65716 56683 131661 36893 36347 50325 120256 548941

- - 3000 187000 190000

roots - - 58000 58000

Total 51060 94504.8 56683 147956.1 54385 101650 128525 388430.5 1023194.4


Harpagophytum spp.

46

Taxonomic notes There are two species in the genus, both with recognised subspecies. Harpagophytum procumbens has

two subspecies: H. procumbens procumbens and H. p. transvaalensis (Setshogo, 2013). Harpagophytum zeyheri has three recognised subspecies: H. z. zeyheri, H. z. schijffii and H. z. subulatum (Krugmann,

2011a).

Conservation status Harpagophytum spp. are creeping prostrate perennials, with annual leaves and large tuberous roots

(Georgiev et al., 2013). The primary tuber is a deep taproot with lateral, often horizontally growing

secondary roots which develop a chain of tubers 4-40 cm long (Strohbach and Cole, 2007). H. procumbens was reported to occur in areas with low annual rainfall (150–500 mm yr

-1) on deep sandy

soils (Stewart and Cole, 2005). It was reported to occur in open woodland and savannah, particularly in

trampled and over-grazed areas such as trails and water-holes where grass and herb cover is low as it

does not compete well with grasses (Catling and Small, 2004; Stewart and Cole, 2005; Hachfeld, 2004).

Harpagophytum zeyheri was reported to occur in areas with higher precipitation (Schneider et al., 2006).

H. procumbens seedling establishment was reported to depend on temperature and rainfall conditions

after germination (Strohbach and Cole, 2007). Natural fluctuations were reported to be dependent on

rainfall (CoP11 Prop 60; Raimondo and Donaldson, 2002). Plants were reported to take between two to

five years to mature and longevity of H. procumbens was estimated by Strohbach and Cole (2007) at over

10 years.

The genus Harpagophytum occurs in southern Africa, with each subspecies having a distinct

distribution. H. procumbens procumbens was reported to occur in South Africa, Namibia and Botswana,

with the subspecies H. p. transvaalensis occurring in a small area of the Limpopo Province of South

Africa (Setshogo, 2013). H. z. zeyheri occurs in northeastern South Africa and was recently recorded in

northern Namibia (Krugmann, 2011a); H. z. schijffii occurs in a very restricted area on the border

between South Africa and Mozambique; and H. z. subulatum occurs in southern Angola, northern

Namibia, Botswana, Zambia and Zimbabwe (Setshogo, 2013).

Populations of Harpagophytum spp. were reported to be patchy and scattered, making estimation of

overall population status difficult (Raimondo and Donaldson, 2002). The area covered by a single

population was reported to rarely exceed 200m x 200m (Hachfield pers. comm. in: CoP11 Prop 60).

According to Nott (1986, in: CoP11 Prop60), populations of H. procumbens normally reached densities of

5-7 plants ha-1, but locally populations of 1 200 plants ha

-1 could be reached. Raimondo and Donaldson

(2002) noted that Harpagophytum procumbens would not be classified as threatened using the IUCN

criteria. The estimated national population of H. procumbens in 2001-2002 was around 56 million plants.

For H. zeyheri, the estimated population was roughly 14 million plants, but these figures were

extrapolated from on fieldwork on approximately 160 sites (Strohbach, 2003).

The main threat to the species was reported to be harvesting (Raimondo and Donaldson, 2002). The

dried and sliced roots of Harpagophytum spp. are used for a variety of medicinal purposes, including

degenerative rheumatoid arthritis, osteoarthritis, tendonitis, kidney inflammation and heart disease

(Stewart and Cole, 2005; Georgiev et al., 2013), and this commodity is exported for trade. The bulk of

international trade historically involved H. procumbens (Raimondo and Donaldson, 2002), and this

species has been the more extensively studied. H. zeyheri was added to the European Pharmacopaoeia in

2003 (Cole, 2003). H. procumbens and H. zeyheri are now both commercially accepted in the

pharmaceutical industry (Stewart and Cole, 2005), and trade in H. zeyheri has become more prevalent in

trade in recent years (Cole, 2013).

Harpagophytum spp.

47

Following the withdrawal of CoP11 Prop 60, three CoP decisions were adopted that aimed to promote

sustainable trade and recognise the importance of the plant as a source of income for marginal

communites in southern Africa. CoP Decision 12.63 directed Range States to provide updates on

implementation of policies and management programmes; Decision 12.64 called on Range States and

importing states to work with the Harpagophytum industry to support management programmes that

promoted sustainable use and the development of communites; and Decision 12.65 urged Range States

to explore how processes and mechanisms in other international treaties could be used to provide

support for sustainable resource use and fair trade.

These decisions were reported to have led to greater regional cooperation between Range States

concerning management of Harpagophytum trade (Setshogo, 2013). The main Range States were

reported to have been working with local communities to develop policies and regulations to protect the

species and determine a sustainable harvest (Stewart and Cole, 2005). Measures to regulate harvest and

trade in Harpagophytum spp. have been developed in Range States in recognition of the vulnerability of

the plant to overexploitation (Setshogo, 2013) and the vulnerability of the communities that depend on

the plant for income (Krugmann, 2011b).

Significant efforts aimed at increasing knowledge of the ecology of Harpagophytum to ascertain

sustainable harvesting levels and methodologies and to investigate feasability of cultivation were

reported (Stewart, 2009; Schneider et al., 2006; Strohbach and Cole, 2007). The genus was reported to be

resilient to harvest of secondary tubers (Stewart, 2009), however Strohbach and Cole (2007) found that

regeneration ability in years after harvest was poorer. Harpagophytum plants have been shown to need

several years growth before they are ready for harvesting (Schneider et al., 2006) and up to four years are

needed for regeneration of the secondary tubers between harvests (Strohbach and Cole, 2007; Nott,

2013).

Aside from trade, the distribution of H. procumbens, and especially H.p. transvaalense was also reported

to have declined due to agricultural expansion, and grazing was also reported as a threat (CoP11 Prop

60). Setshogo (2013) reported that H. procumbens was likely to disappear due to bush encroachment in

overgrazed farmland or communal land, because of its low competitive ability. Harpagophytum spp. are

considered a nuisance to livestock farmers and were reported to be frequently removed from grazed

fields (Stewart and Cole, 2005; Catling and Small, 2004; Hachfeld and Schippmann, 2000), as the hooked

fruits can injure livestock (Catling and Small, 2004).

In Namibia, H. procumbens occurs extensively in central and southeastern areas where rainfall is approx

150-300 mm yr-1 (Krugmann, 2011a). H. zeyheri was reported to occur in the northern areas near the

borders with Angola and Zambia (Krugmann, 2011a; Setshogo, 2013). H. procumbens was previously

abundant throughout its native range but was reported to have disappeared or had been greatly reduced

in many parts of Namibia (Catling and Small, 2004). Krugmann (2011a) noted that most harvesting had

taken place in the communal areas of four Regions: Omaheke, Otjozondjupa, Caprivi and Kavango, and

that outside of these areas, significant Harpagophytum populations could be found on wide stretches of

private farmland and in protected areas which remained largely unexploited.

Namibia was reported to have supplied the bulk of Harpagophytum on the international market over the

last two decades (Setshogo, 2013) and unsustainable harvesting practices were reported to be widespread

(Raimondo and Donaldson, 2002; Schneider et al., 2006). According to CoP11 Proposal 60 (various

sources), annual exports of H. procumbens from Namibia were around 28 000 kg in 1973, and then

averaged around 140 000 kg during the 1970s and 1980s (for years for which data was available), with

trade levels rising in the 1990’s to 610 000 kg reported in 1998.

Harpagophytum spp.

48

Production of H. zeyheri from the Caprivi Region (which has consistently produced the greatest volumes

of Harpagophytum) rose from just under 50 tonnes in 2010, to almost 250 tonnes (250 000 kg) in 2011

(Möller, 2013).

Trade and impact on populations of H. zeyheri are unknown particularly because of unregulated trade

from Angola (Johnson, 2013) and Zambia (Möller, 2013; Nyirenda, 2013). Tubers of H. zeyheri were

reported to be mixed with H. procumbens in areas where the two species occur together such as in

northern Namibia (Raimondo and Donaldson, 2002).

Krugmann (2011a) listed a number of risk factors that could lead to overexploitation of Harpagophytum spp. populations in local populations, including the fragmented nature of the industry and difficulties of

regulating supply chains, in addition to the poverty, marginalisation and exploitation of the primary

harvesters, and consequent lack of collective action at local, national and regional levels (Krugmann,

2011a). Within Namibia, the trade chain from harvest to export has evolved as a largely informal

unorganized structure, involving up to 8 000 harvesters and primary processors and up to 200 traders

and five exporters (Krugmann, 2011b).

Both Harpagophytum spp. were listed as protected species under Schedule 9 of the Nature Conservation

Ordinance of 1975 in Namibia (CoP11 Prop. 60; Strohbach and Cole, 2007). From 1987 onwards, permits

were required for commercial trade of Harpagophytum (CoP11 Prop.60; Cole, 2013).

The vast range of Harpagophytum spp. in Namibia was reported to make management of the resource

and enforcement of policy difficult (Raimondo and Donaldson, 2002). Implementation of sustainable

harvesting methods across Namibia were reported to require effective application and enforcement of

policy and regulatory instruments which were noted as challenging because of the remoteness of many

of the areas where harvesters and traders operate, and low levels of education and resources among

many of the harvesters (Krugmann, 2011a).

However, a number of management measures have been introduced. At the 14th Meeting of the Plants

Committee (2004), Namibia reported undertaking surveys of the available resource (Strohbach, 2003),

socio-economic factors (Grote, 2003), and market conditions in 2002 to establish baseline for the status

of Harpagophytum in Namibia (density and distribution) and inform support for management of trade

(PC 14 Inf. 14).

The Namibian Ministry of Environment and Tourism (MET) introduced the National Policy on

Utilisation of Devil’s Claw in 2010 (NPUDC) replacing draft policy that had been in place for 10 years

(Krugmann, 2011b). The NPUDC sets out rules intended to ensure sustainable harvest of Harpagophytum

in Namibia (Nott, 2013). Harvest levels were based in part on the studies of Strohbach and Cole (2007),

who reported that plants should be at least three years old when first harvested and plants should be left

to recover for at least three years to allow for tuber regeneration (Strohbach and Cole, 2007).

The MET is reponsible for monitoring permiting and trade in Harpagophytum (Möller, 2013). All

exporters and traders must have permits and complete reports to the MET (Nott, 2013). All harvesters

registered with permitted community-based organisations receive training in sustainable harvesting and

processing methods (Nott, 2013). It was reported that there are still issues with illegal harvest of

Harpagophytum spp. as, between 2008 and 2011 around half of the Harpagophytum spp. exported was

not legally harvested (Möller, 2013). In addition to the NPUDC, efforts are being made to improve the

organisation of the industry in Namibia, including training in sustainable harvesting and processing to

improve the quality of harvested and dried material (Krugmann, 2011b). The Devil’s Claw Enviromental

Management Plan (DCEMP) (Krugmann, 2011b) sets out the practical measures to mitigate negative

environmental and social impacts of harvesting Harpagophytum spp. through strengthening the

organisation of producers and processors, which are expected to produce positive environmental and

Harpagophytum spp.

49

social impacts (Krugmann, 2011b). Measures to mitigate negative impacts for harvesting set out in the

DCEMP included: capacity building and training for suitable Producer Processer Organisations;

technical assistance and mentoring; provision of equipment knives, nets, bags, etc; implementation of a

Gender and Social Integration Plan (den Adel, 2010).

According to Krugmann (2011a) information about the changing spatial and temporal patterns of

Harpagophytum harvesting activity and its impacts on each species is lacking, due to the largely

informal, unorganized nature of the Harpagophytum spp. trade (Krugmann, 2011a). Only 10% of

Harpagophytum spp. harvested in 2010 were gathered using sustainable harvesting methods (Krugmann,

2011a). The NPUDC and the DCEMP, if fully implemented, should address these issues by helping to

manage the supply, control illegal imports and aid tracability and sustainabilty of wild-harvested

Harpagophytum spp.

However, the risk of possible commercial over-utilisation of Harpagophytum resources, was not thought

to pose a significant threat to national populations of Harpagophytum spp. or the survival of the species

(Krugmann, 2011a).

References den Adel, S. 2010. Gender and Social Integration Plan, MCA-N Indigenous Natural Products Producer and

Processor Organisations Sub-Activity Report Number 3. Millenium Challenge Account Namibia. Windhoek. 42 pp.

Catling, P.M. and Small, E. 2004. Blossoming treasures of biodiversity. Biodiversity, 5(3): 26–30. Cole, D. 2013. Overview of Devil’s Claw and workshop goals. In: Proceeding of the Namibian Devil’s Claw

Workshop. Windhoek. 6–7. Cole, D. 2003. The impact of certification on the sustainable use of Devil’s Claw (Harpagophytum

procumbens) in Namibia. 34 pp. Georgiev, M.I., Ivanovska, N., Alipieva, K., Dimitrova, P. and Verpoorte, R. 2013. Harpagoside: from

Kalahari Desert to pharmacy shelf. Phytochemistry, 92: 8–15. Grote, K. 2003. The increased harvest and trade of Devil’s Claw (Harpagophytum procumbens) and its

impacts on the peoples and environment of Namibia , Botswana and South Africa. Global Facilitation Unit for Underutilized Species, Maccarese. 1–30 pp.

Hachfeld, B. 2004. Ecology and utilisation of the medicinal plant Harpagophytum procumbens (Burch.) DC. ex Meissn. (Pedaliaceae) in southern Africa. Universität Hamburg.

Hachfeld, B. and Schippmann, U. 2000. Conservation data sheet 2 Harpagophytum procumbens. Medicinal Plant Conservation, 6: 4–9.

Johnson, S. 2013. SAREP’s role in supporting Devil's Claw in southeastern Angola. In: Proceedings of the Namibian Devil’s Claw Workshop. Windhoek. 17–18.

Krugmann, H. 2011a. Indigenous Natural Products Producer and Processor Organisations Sub-Activity EIA for Devil’s Claw. Millennium Challenge Account Namibia. Windhoek. 101 pp.

Krugmann, H. 2011b. Indigenous Natural Products Producer and Processor Organisations Sub-Activity Environmental Management Plan for Devil’s Claw. Millenium Challenge Account Namibia. Windhoek. 44 pp.

Möller, W. 2013. MET trade statistics and permits. In: Proceedings of the Namibian Devil’s Claw Workshop. 25–28.

Nott, K. 1986. A survey of the harvesting and export of Harpagophytum procumbens and

Harpagophytum zeyheri in SWA/Namibia. – Unpublished Report, Etosha Ecological Institute,

P.O. Okaukuejo, Namibia. Nott, K. 2013. NPUDC refresher training. In: Proceedings of the Namibian Devil’s Claw Workshop.

Windhoek. 20–25. Nyirenda, M. 2013. The status of Devil’s Claw in Zambia. In: Proceeding of the Namibian Devil’s Claw

Workshop. Windhoek. 15–16.

Harpagophytum spp.

50

Raimondo, D. and Donaldson, J. 2002. The trade, management and biological status of Harpagophytum spp. in southern African range states. A Report submitted to the 12th meeting of the CITES Plants Committee. 20 pp.

Schneider, E., Sanders, J. and Willert, D.V.O.N. 2006. Devil’s Claw (Harpagophytum procumbens) from southern Africa. In: Bogers, R.J., E, C.L. and D, L. (Eds.). Medicinal and Aromatic Plants. 181–202.

Setshogo, M.P. 2013. To list or not to list? Arguments for and against listing Harpagophytum species on Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Journal of Medicinal Plants Research, 7(48): 3492–3498.

Stewart, K.M. 2009. Effects of secondary tuber harvest on populations of devil’s claw (Harpagophytum procumbens) in the Kalahari savannas of South Africa. African Journal of Ecology, 48: 146–154.

Stewart, K.M. and Cole, D. 2005. The commercial harvest of Devil’s claw (Harpagophytum spp.) in southern Africa: the devil's in the details. Journal of Ethnopharmacology, 100(3): 225–36.

Strohbach, M. 2003. National Resource Survey. The Namibian National Devil’s Claw Situation Analysis. Strohbach, M. 2007. Reducing the harvesting impact on Harpagophytum procumbens populations in the

Omaheke Region, eastern Namibia. South African Journal of Botany, 73(2): 315. Strohbach, M. and Cole, D. 2007. Population dynamics and sustainable harvesting of the medicinal plant

Harpagophytum procumbens in Namibia. Federal Agency for Nature Conservation, Bonn. 1–61 pp.

Appendix 1

51

Appendix 1 Introduction to the Analysis of the European Union Annual Reports to CITES UNEP-WCMC undertakes an annual Analysis of the European Union and candidate countries’ annual reports to CITES. The Analysis examines patterns of trade into the European Union and candidate

countries, trade in groups of particular note, possible transgressions of suspensions and negative

opinions, exports of native species, etc.

As part of the 2012 Analysis, imports reported by the EU (and candidate countries) as wild-sourced,

ranched, source ‘unknown’ or source ‘blank’ were analysed to identify noteworthy patterns of trade

according to five criteria. These criteria were designed to identify:

1. High volume trade in 2012

2. Globally threatened and near threatened species traded at relatively high volumes in 2012

3. Sharp increase in trade in 2012

4. General long term increases or decreases in trade between 2003 and 2012

5. Long term variability in trade between 2003 and 2012.

Imports were considered to be ‘high volume’ according to thresholds which were determined by

taxonomic group and CITES Appendix (Table 1). In order to account for threat status, the Appendix I

threshold was also applied to Appendix II and III species considered to be threatened or near threatened

by the IUCN (Critically Endangered, Endangered, Vulnerable and Near Threatened in the IUCN Red

List).

Table 1. Minimum number of wild, ranched, source ‘unknown’ and source ‘blank’ individuals imported in 2012 needed to qualify for selection on the basis of high trade volume.

Taxonomic group CITES Appendix / IUCN Red List status

I II III I/II/III (kg)

CR, EN, VU, NT*

- CR, EN, VU, NT*

- CR, EN, VU, NT*

-

Mammals 50 50 5000 50 25 000 50 5000

Birds 50 50 5000 50 25 000 50 5000

Reptiles 50 50 25 000 50 50 000 50 25 000

Amphibians 50 50 25 000 50 50 000 50 25 000

Fish 50 50 25 000 50 — 50 25 000

Invertebrates (non-corals) 250 250 25 000 250 50 000 250 25 000

Corals — 10 000 25 000 10 000 50 000 10 000 25 000

Plants (non-tree) 250 250 25 000 250 50 000 250 25 000

Plants (trees) 250 m³ 250 m³ 500 m³ 250 m³ 2500 m³ 2500 25 000 * CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Near Threatened in IUCN Red List (http://www.iucnredlist.org/)

The ‘sharp increase’ criterion was designed to determine if there was a sharp increase in importer-

reported wild-sourced imports in 2012, compared with the average level of imports between 2007 and

2011. Species that, despite a sharp increase in trade in 2012, were still only traded in very low volumes

(i.e. less than 5 per cent of the levels listed in Table 1) were omitted.

Appendix 1

52

The ‘overall increase’ criteria took into account more general trends over the period 2003-2012 by

calculating the slope of a best-fit linear function to the trade data, with a large positive slope indicating a

significant increase in trade levels over time.

To account for highly variable trade that may not be picked up by the other criteria, the coefficient of

variation was calculated for imports over a ten-year period (2003-2012) and species showing high

variation over this period were selected.

Appendix 2

53

Appendix 2 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

X Specimens taken in “the marine environment not under the jurisdiction of any State”

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

Documents

Review of species selected on the basis of the Analysis of ...ec.europa.eu/environment/cites/pdf/reports/Review of species... · Review of species selected on the basis of the Analysis