Research Article |
Corresponding author: Sarah Heinrich ( sarah.heinrich@adelaide.edu.au ) Academic editor: Matthias Halwart
© 2021 Sarah Heinrich, Lalita Gomez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Heinrich S, Gomez L (2021) India’s use of CITES Appendix III. Nature Conservation 44: 163-176. https://doi.org/10.3897/natureconservation.44.63688
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India is one of the few countries to have made extensive use of Appendix III of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), compared to other Parties to the Convention. Here we examine India’s use of Appendix III and illustrate its benefits and limitations, using examples of species listed by India in Appendix III. Since its ratification of CITES in 1976, India has listed 39 taxa in Appendix III, 27 species and six subspecies listings of which are still current. Through the listings, important international trade data was gathered, some of which have supported the decision for application to a different CITES Appendix with stricter trade controls. However, the majority of the species have been listed for more than 30 years and a re-evaluation of their listing status and suitability for Appendix III may be warranted. The same applies to the reservations entered by several Parties. We provide recommendations on how to make some of the current listings more effective and encourage other Parties to evaluate their native, non-CITES listed species and, if warranted, to make use of Appendix III to contribute to the conservation of their native wildlife.
conservation, policy, threatened species, wildlife trade
Global biodiversity is facing a crisis with many species on a rapid path to extinction (
Appendix III is seldom used, with under 1% of all CITES taxa listed in Appendix III (https://cites.org/eng/disc/species.php). In this paper we focus on Appendix III to explore how it has been used in practice, using India as a case study, which in comparison to other Parties, has the most listings in Appendix III (Fig.
For the right candidate species, Appendix III can have multiple benefits, including: i) a comparatively easier listing and permitting process; ii) the provision of a legal basis for law enforcement bodies in consumer countries to seize illegal specimens; iii) monitoring of trade patterns and volumes of listed species; as well as iv) the prevention of overexploitation of at-risk species (
Appendix III follows distinct listing and permitting procedures compared to Appendix I and II. For a species to be listed, de-listed or moved between Appendix I and II the Parties meet every 3 years at the Conference of the Parties (CoP) and each change in species status requires support from a two third majority of the Parties to be accepted (CITES Article XV; https://cites.org/eng/disc/text.php#XV). In contrast, an Appendix III listing is comparatively easier and can be proposed unilaterally by any Party at any time by simply notifying the CITES Secretariat. The submitting Party is asked to make any domestic laws and regulations (and interpretations thereof) applicable to the protection of the proposed species available to the Secretariat. They also need to submit any changes to the legislation (if any) for as long as the species is listed in Appendix III (CITES Article XVI; https://cites.org/eng/disc/text.php#XVI). It is also possible to only list certain parts or derivatives of a species, or only national populations; however, this is not generally recommended as it may complicate enforcement efforts considerably. Any Party that opposes the listing can enter a Reservation. If not otherwise regulated through national legislation (see e.g., Council Regulation (EC) No 338/97 for the case of the European Union (EU)), the Party is then treated as a non-Party in regards to the species it has entered a Reservation for.
In addition to the comparatively easier listing process, the permit requirements for Appendix III are less strict. As such, export permits are only required from the listing Party, while all other Parties need to issue a certificate of origin for the species in question. In the case of a re-export from any country, a re-export permit needs to be issued (CITES Article V; https://cites.org/eng/disc/text.php#V). However, in contrast to species listed in Appendix I and II, non-detriment findings (NDF) are not required for species listed in Appendix III prior to export; not even from the country that listed the species (CITES Article V; https://cites.org/eng/disc/text.php#V). This significantly reduces the workload for CITES Scientific Authorities and results in less bureaucracy associated with trade in Appendix III species. On the other hand, it also leads to less control and efficacy, as NDFs are an important tool for ensuring the sustainability of trade.
One of the few countries to have used Appendix III extensively in the past compared to other Parties is India (Fig.
In the context of CITES, India is considered a category 2 country under the CITES National Legislation Project (https://cites.org/eng/legislation/National_Legislation_Project), meaning that only 1 – 3 of the four requirements for effective implementation of CITES have been met, as outlined in Res. Conf. 8.4 (Rev. CoP15). Essentially, India has no national law to implement CITES (
The international trade of wildlife in India as it pertains to CITES listed species is governed under several laws including the Wild Life Protection Act 1972, Foreign Trade Act 1992, and Foreign Trade Policy. The main provisions of CITES are enforced through the Customs Act 1962. The principle law governing wildlife protection on a national basis is the Wild Life Protection Act 1972, which has been amended several times, i.e., in 1991, 2002, 2003 and 2006, e.g., to include new species, higher penalties, and stronger protection. Native wildlife is protected to varying degrees under Schedules I-VI of this Act. In very general terms, it prohibits the hunting, killing, unlicensed possession, unlicensed transport, and any mode of transfer, apart from inheritance, of protected species or products thereof, such as trophies, meat, animal articles, etc. This includes domestic and international commercial trade in wild individuals of protected species unless specifically permitted otherwise. There are provisions within the Act for certain exceptions, e.g., the killing of a protected species is permissible if it constitutes a threat to life; hunting permits are given if a species is considered a threat to property (e.g., crops); or export of species for scientific research/ exchange between zoos, etc. However, the Wild Life Protection Act does not include governance of non-native species and this severely impedes efforts to enforce the law, including the prosecution or penalties associated with the smuggling of non-native species within and across India’s borders. The Foreign Trade Act 1992 essentially makes provisions for prohibiting, restricting and/or regulating goods subject to import and export including wildlife. Under the Foreign Trade Policy, governed by the Act, the principles on which wildlife and their products that can, or are prohibited to be, imported or exported are provided based on consultation with the CITES Management Authority, which is in turn enforced through the Customs Act 1962 that has the power to prohibit the importation and exportation of goods, including wildlife.
In order to explore the use of Appendix III we collated a list of taxa that have been listed by India in Appendix III at any point in time, based on the history of CITES listings (www.speciesplus.net). We focussed on three of those species i.e., Malabar civet (Viverra civettina), Siberian weasel (Mustela sibirica), and Red fox (Vulpes vulpes), by summarising trade data for these species to further assess and exemplify the benefits, suitability and challenges of listing species in Appendix III.
Trade data were downloaded in November 2020 from the CITES trade database (trade.cites.org). Law Enforcement Management Information System (LEMIS) data for the Malabar civet were obtained through a Freedom of Information Request. Species native ranges were obtained from the CITES species checklist (www.speciesplus.net) and their respective IUCN status from the IUCN Red List (www.iucnredlist.org). We note that we refer to the listed taxa using the taxonomy used in CITES, but we acknowledge that this may not necessarily reflect the most up-to-date taxonomic information.
Since its ratification of the Convention in 1976, India has listed 33 species and six subspecies in Appendix III. All of them were first listed before 1990 and since their listing, six of the 33 species have subsequently been moved to Appendix II or I. Currently, India still has 27 species and six subspecies listed in Appendix III (Table
It has been remarked that endemic species are especially well suited for a listing in Appendix III, as the opportunity for laundering the species through other range states is essentially non-existent (
In the case of India, only four of the 33 currently listed (sub-) species are Indian endemics. This includes the Malabar civet, which has been listed in Appendix III since 1989. The Malabar civet is Critically Endangered and only occurs in the Western Ghats in the south of India (
Further, if looking at trade records of Malabar civets recorded in LEMIS, none of these match the trade records recorded in CITES (and vice versa; Table
An Appendix III listing can have further benefits, for example, through the recording of international trade data – crucial information that is often missing for many traded non-CITES wildlife species (
For example, six species that had been listed by India in Appendix III were subsequently transferred to Appendix II, i.e., Monocled Cobra (Naja kaouthia), Spectacled Cobra (Naja naja), Central Asian Cobra (Naja oxiana), King Cobra (Ophiophagus hannah), and Oriental Ratsnake (Ptyas mucosus); and Appendix I, i.e., Sloth Bear (Melursus ursinus). Among the central arguments supporting the inclusion of the five snake species to Appendix II was trade data gathered while the species were included in Appendix III, as well as illegal trade data supporting the transfer (CoP7 Proposals 45, 46, and 47; https://cites.org/eng/cop/07/prop/index.php). The five snake species were transferred to Appendix II approximately six years after their initial listing in Appendix III, while the Sloth bear was moved to Appendix I approximately two years after its initial listing in Appendix III (Table
The (sub-) species currently and historically listed by India in CITES Appendix III, including their IUCN status (if assessed, with CR = Critically Endangered, DD = Data Deficient, LC = Least Concern, NT = Near Threatened, VU = Vulnerable), potential transfers to different Appendices (App I, II), current reservations by the Parties, and Protection Status in India (indicating the Schedule (Sch) of the Wild Life Protection Act 1972 under which the species is listed).
Family | Scientific name | Common name | IUCN status | App III addition | App II addition | App I addition | Current reservations | Protection status in India |
---|---|---|---|---|---|---|---|---|
Canidae | Canis aureus | Golden Jackal | LC | 1989 | – | – | 2 countries | Sch II, Part II |
Vulpes bengalensis | Bengal Fox | LC | 1989 | – | – | – | Sch II, Part II | |
Vulpes vulpes griffithi | 1989 | – | – | 25 countries | Sch II, Part II | |||
Vulpes vulpes montana | 1989 | – | – | 24 countries | Sch II, Part II | |||
Vulpes vulpes pusilla | 1989 | – | – | 25 countries | Sch II, Part II | |||
Colubridae | Atretium schistosum | Olive Keelback Water Snake | LC | 1984 | – | – | – | Sch II, Part II |
Cerberus rynchops | South Asian Bockadam | LC | 1984 | – | – | – | Sch II, Part II | |
Xenochrophis piscator | Checkered Keelback | 1984 | – | – | – | Sch II, Part II | ||
Xenochrophis schnurrenbergeri | Bar-necked Keelback | 1984 | – | – | – | Sch IV | ||
Xenochrophis tytleri | Tytler’s Keelback | 1984 | – | – | – | Sch IV | ||
Ptyas mucosus | Oriental Ratsnake | 1984 | 1990 | – | – | Sch II, Part II | ||
Elapidae | Naja kaouthia | Monocled Cobra | LC | 1984 | 1990 | – | – | Sch II, Part II |
Naja naja | Spectacled Cobra | 1984 | 1990 | – | – | Sch II, Part II | ||
Naja oxiana | Central Asian Cobra | DD | 1984 | 1990 | – | – | Sch II, Part II | |
Ophiophagus hannah | King Cobra | VU | 1984 | 1990 | – | – | Sch II, Part II | |
Herpestidae | Herpestes edwardsi | Indian Grey Mongoose | LC | 1989 | – | – | – | Sch II, Part II |
Herpestes fuscus | Brown Mongoose | LC | 1989 | – | – | – | Sch II, Part II | |
Herpestes smithii | Ruddy Mongoose | LC | 1989 | – | – | – | Sch II, Part II | |
Herpestes urva | Crab-eating Mongoose | LC | 1989 | – | – | – | Sch II, Part II | |
Herpestes vitticollis | Stripe-necked Mongoose | LC | 1989 | – | – | – | Sch II, Part II | |
Herpestes javanicus auropunctatus1 | LC | 1989 | – | – | – | Sch II, Part II | ||
Mustelidae | Martes flavigula | Yellow-throated Marten | LC | 1989 | – | – | – | Sch II, Part II |
Martes gwatkinsii | Nilgiri Marten | VU | 1989 | – | – | – | Sch II, Part II | |
Mustela altaica | Altai Weasel | NT | 1989 | – | – | 24 countries | Sch II, Part II | |
Mustela kathiah | Yellow-bellied Weasel | LC | 1989 | – | – | 24 countries | Sch II, Part II | |
Mustela sibirica | Siberian Weasel | LC | 1989 | – | – | 24 countries | Sch II, Part II | |
Martes foina intermedia | 1989 | – | – | 3 countries | Sch II, Part II | |||
Mustela erminea ferghanae | 1989 | – | – | 24 countries | Sch I, Part I | |||
Sciuridae | Marmota caudata | Long-tailed Marmot | LC | 1989 | – | – | – | Sch II, Part II |
Marmota himalayana | Himalayan Marmot | LC | 1989 | – | – | – | Sch II, Part II | |
Ursidae | Melursus ursinus | Sloth Bear | VU | 1988 | – | 1990 | – | Sch I, Part I |
Viperidae | Daboia russelii | Russell’s Viper | 1984 | – | – | – | Sch II, Part II | |
Arctictis binturong | Binturong | VU | 1989 | – | – | – | Sch I, Part I | |
Paguma larvata | Masked Palm Civet | LC | 1989 | – | – | – | Sch II, Part II | |
Paradoxurus hermaphroditus | Common Palm Civet | LC | 1989 | – | – | – | Sch II, Part II | |
Paradoxurus jerdoni | Brown Palm Civet | LC | 1989 | – | – | – | Sch II, Part II | |
Viverra civettina | Malabar Civet | CR | 1989 | – | – | – | Sch I, Part I | |
Viverra zibetha | Large Indian Civet | LC | 1989 | – | – | – | Sch II, Part II | |
Viverricula indica | Small Indian Civet | LC | 1989 | – | – | – | Sch II, Part II |
Trade data reported to CITES for the Malabar civet (Viverra civettina) from 1989 – 2020. AU = Australia, CM = Cameroon, NL = The Netherlands, NZ = New Zealand, PH = The Philippines, PL = Poland, SG = Singapore, TG = Togo, US = United States of America, VN = Vietnam.
Year | Importer | Exporter | Origin | Source | Quantity (I/E) | Commodity | Purpose |
---|---|---|---|---|---|---|---|
1992 | US | PH | VN | Wild | 1/– | Skin | – |
1995 | US | SG | – | Seized | 1/– | Body | Commercial |
1998 | US | VN | – | Wild | –/135 | Live | Commercial |
2010 | PL | CM | – | Wild | 1/– | Trophy | Hunting |
2014 | NL | TG | – | Wild | –/9 | Skins | Commercial |
2015 | NL | TG | – | Wild | –/25 | Live | Commercial |
2015 | NZ | AU | – | Wild | –/1 | Skin | Personal |
2015 | NZ | AU | – | Wild | –/1 | Skull | Personal |
2015 | US | TG | – | Wild | –/8 | Live | Commercial |
The 33 taxa that have been listed by India, and which are still included in Appendix III today, have been listed for over 30 years each and an evaluation of the effectiveness of the listings and the ongoing suitability of the species may be warranted. Ideally, Appendix III should be an interim, not a long-term solution. Assistance for the review of Appendix III species can be sought from the Animals and Plants Committees of CITES (see Res. Conf 9.25 (Rev CoP18), paragraph 5) and Parties are urged to undertake these reviews at regular intervals (Res. Conf. 9.25 (Rev CoP18), paragraph 6).
For example, another species currently listed in Appendix III by India that would potentially benefit from a transfer to Appendix II is the Siberian weasel (Mustela sibirica) (see Res. Conf 9.24 (Rev CoP17); https://cites.org/sites/default/files/document/E-Res-09-24-R17.pdf for Appendix II criteria). It has a wide distribution, occurring in at least 12 countries and is currently listed as Least Concern by the IUCN Red List (
One of the often-mentioned downfalls of a listing in Appendix III is that it may become ineffective for species with a large native range, spanning several countries, as e.g., the potential for laundering is very high, and the listing is often hindered by a lack of cooperation and communication between the relevant range states (
The native range of some of the other listed species involves several (i.e., more than 10) countries and it is unlikely that all of them would join the listing of the species in question. Especially if the conservation situation for the species differs in the many different range states. They may not be perceived as threatened in some countries, while the situation may be different in other countries. For example, countries have entered reservations for 26 of India’s listed taxa throughout history, nine of which are still current. It is noteworthy that all current reservations are exclusively for fur-bearing animal species of varying commercial value, and the majority of the reservations (five out of nine) were entered for subspecies. Three of these are subspecies of the Red fox (Vulpes vulpes). The number of extant fox taxa in India has been of much debate, including subspecies of the Red fox (
It could be argued that the inclusion of subspecies is relevant, as they can essentially be treated as ‘endemics’, depending on the actual geographic range of the subspecies in question. However, one issue of listing subspecies and/or national populations in CITES generally, but Appendix III in particular, is the potential for misidentifications, especially for very similar looking (sub-)species, which makes law enforcement extremely difficult (
Apart from the difficulties of identifying subspecies, another possibility for why trade may not have been captured for the Red fox subspecies is that trade for personal purposes in Appendix III species does not require any documentation under CITES (https://cites.org/eng/imp/Exemptions_and_special_procedures). It is the only ‘true’ exemption that exists in CITES, as opposed to any of the other exemptions, e.g., captive bred, or pre-convention specimens, which require special procedures and documentation (Res. Conf. 12.3 (Rev. CoP18); https://cites.org/sites/default/files/document/E-Res-12-03-R18.pdf). It is possible for Parties to take stricter domestic measures in regards to the personal and household effects exemption (Res. Conf. 13.7 (Rev.CoP17); https://cites.org/eng/res/13/13-07R16.php), but not many Parties do for Appendix III species. It is therefore possible that legal trade in Appendix III species does occur, but is not recorded in CITES (see also
India has listed 33 species and six subspecies in Appendix III, 33 listings of which are still current. The listings have led to important insights into international trade; however, the majority of the species have been listed for more than 30 years and a re-evaluation of their listing status and suitability for Appendix III is warranted. The same applies to the reservations entered by several Parties, as it appears that at least some of the species that Parties have entered reservations for are, in fact, heavily traded internationally and may even require better protection and regulation from international trade than is currently the case. Some of the taxa listed by India appear to be well suited for an Appendix III listing, while others may benefit from being transferred to a different Appendix, or could potentially be removed from Appendix III, for example if no considerable international trade occurs. The assessments should be made on a case-by-case basis, and evaluated based on the recommendations made in CITES Res. Conf. 9.25 (Rev.CoP18).
While species should fit certain criteria for a listing to be effective, Appendix III can still have advantages even if species are not ‘ideal’ candidates. For example, international trade data is recorded, which is crucial information that is often lacking for non-CITES species. For the right candidate species, Appendix III can have considerable benefits, and other Parties should consider its use for their native wildlife species, especially as an interim solution. However, despite a listing in CITES and the legal protection that is granted through the Convention, illegal trade may still occur. A CITES listing, whether in Appendix I, II, or III, can only contribute to species conservation if Parties implement and enforce the requirements of the Convention.
We thank WWF-Netherlands for their generous support to the Monitor Conservation Research Society to carry out this research. C. R. Shepherd is thanked for his review of an earlier draft of the manuscript. We also thank Belinda Wright and Tito Joseph from WPSI for useful information on the wildlife trade in India.
Table S1
Data type: Government trade records
Explanation note: Trade data reported in LEMIS for the Malabar civet (Viverra civettina) from 2000 – 2019.