Illegal Trade of the Psittacidae in Venezuela

Illegal trade of the Psittacidae in Venezuela

A DA S ÁNCHEZ-MERCADO,MARIANNE A SMÜSSEN,JON P AUL R ODRÍGUEZ L ISANDRO M ORAN,ARLENE C ARDOZO-URDANETA and L ORENA I SABEL M ORALES

Abstract Illegal wildlife trade is one of the major threats to trade involves avian species, poached to supply both domes- Neotropical psittacids, with nearly % of species targeted tic and international demand for pets (Rosen & Smith, for the illegal pet trade. We analysed the most comprehen- ). Among birds, Neotropical psittacids are of primary sive data set on illegal wildlife trade currently available for conservation concern, with nearly % of species affected Venezuela, from various sources, to provide a quantitative by poaching for the illegal pet trade (Olah et al., ). assessment of the magnitude, scope and detectability of The data used to measure the magnitude of the illegal pet the trade in psittacids at the national level. We calculated trade in psittacids have come from four main sources: seiz- a specific offer index (SO) based on the frequency of ure records and surveys of trappers (Cantú Guzmán et al., which each species was offered for sale. Forty-seven species ), literature reviews (Pires, ; Alves et al., ), dir- of psittacids were traded in Venezuela during –,of ect observation in markets (Herrera & Hennessey, ; which  were non-native. At least , individuals were Gastañaga et al., ; Silva Regueira & Bernard, ), traded, with an overall extraction rate of , individuals and observation of the proportion of nest cavities poached per year ( years of accumulated reports). Amazona (Wright et al., ; Pain et al., ; Zager et al., ). ochrocephala was the most frequently detected species Each source has a unique geographical and taxonomic (SO = .), with the highest extraction rate (, indivi- coverage and evaluates different aspects of the market duals per year), followed by Eupsittula pertinax (SO = .) chain. Studies using a variety of sources are less frequent and Amazona amazonica (SO = .). Amazona barbaden- (Gavin et al., ), although a combination of sources sis, Ara ararauna and Ara chloropterus were the fourth most could probably provide a better insight into the magnitude frequently detected species (SO = .–.). Eleven spe- and scope of illegal activities, particularly in countries that cies were involved principally in domestic trade (. %of lack the infrastructure to formally monitor illegal wildlife records). Our approach could be the first step in developing trade (Kaufmann et al., ). a national monitoring programme to inform national policy In the Neotropics, Venezuela ranks second in psittacid on the trade in psittacids. Patterns and numbers provided species diversity (Rodríguez et al., ). Declining trends may be used to update the official list of threatened species, have been reported for  of the  psittacid species that and could also be used in planning conservation actions. occur there, and six are considered to be threatened (Supplementary Table S). The primary threats to Keywords Birds, conservation, illegal wildlife trade, par- Venezuelan psittacids are capture for the pet trade (both do- rots, pet trade, Venezuela mestic and international), and the destruction of nesting Supplementary material for this article is available at and feeding habitat by urban development (Rodríguez https://doi.org/./SX et al., ). Recent evidence suggests that even the most widespread psittacids of the genus Amazona may have undergone declines in their distribution (Ferrer-Paris et al., ). A previous review of trade in Venezuelan Introduction Psittacidae reported that at least  species were traded fre-  llegal wildlife trade is one of the major threats to global quently, both domestically and internationally, and of  Ibiodiversity, generating a black market valued at USD these were traded heavily (Desenne & Strahl, ). – billion per year (Wyler & Sheikh, ). Most of this However, with no quantitative measure of the capture frequency or extraction rates, the use of this information for monitoring purposes is limited. A more quantitative assess- ADA SÁNCHEZ-MERCADO (Corresponding author), LISANDRO MORAN,ARLENE ment, but with a local focus, estimated that Forpus passeri- CARDOZO-URDANETA* Centro de Estudios Botánicos y Agroforestales, Instituto nus, Eupsittula pertinax and Psittacara wagleri were the Venezolano de Investigaciones Científicas, Apartado 20632, Caracas 1020-A, Venezuela. E-mail [email protected]/[email protected] most frequently traded psittacids (Marín-Espinoza et al.,  MARIANNE ASMÜSSEN,JON PAUL RODRÍGUEZ Centro de Ecología, Instituto ). Venezolano de Investigaciones Científicas, Caracas, Venezuela Here we analyse the most comprehensive data set on il-

LORENA ISABEL MORALES Fundación Vida y Mar, Maracaibo, Venezuela legal wildlife trade currently available in Venezuela, gath- *Also at: Fundación Vida y Mar, Maracaibo, Venezuela ered from various sources. We take into account data Received  February . Revision requested  May . limitations and biases to provide a quantitative assessment Accepted  July . First published online  November . of the magnitude, scope and detectability of the trade in

Oryx, 2020, 54(1), 77–83 © 2017 Fauna & Flora International doi:10.1017/S003060531700120X Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.8, on 27 Sep 2021 at 17:51:06, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531700120X 78 A. Sánchez-Mercado et al.

psittacids at the national level. Specifically, we evaluate () Data compilation the number of species involved in trade, () the magnitude of the trade in terms of number of reports per year and num- We defined as illegal all take without permits of undomes- ber of individuals traded per year, by species, and () the ticated terrestrial psittacid species from protected or private level of complementarity among data sources. Our approach areas, including unlicensed harvesting of eggs or juveniles of systematic data compilation from various sources, taking and domestic and international trade of live specimens  into account their limitations and heterogeneity, could be (Sánchez-Mercado et al., ). We categorized records of applicable in other countries with a tradition of commercial illegal trade as domestic or international. The domestic wildlife use and a lack of infrastructure for wildlife-use mon- trade category included records of whole specimens or itoring (Kaufmann et al., ). their parts offered for sale or barter to local buyers, either directly by trappers or by intermediate dealers who obtained items from trappers or other local intermediates. The inter- Methods national trade category included sales by trappers or intermediates to buyers abroad (Sánchez-Mercado et al., ). Study area and legal framework We included all uses described for a given report; for ex- Our study area spans the entire Venezuelan territory ample, if a trapper captured a parrot and sold it in a local  (. km ; Aguilera et al., ). Wildlife administration market or to a neighbour, this was recorded as domestic is under the jurisdiction of the Ministry for Ecosocialism and trade, but if the trapper sold the parrot to a local intermedi- Water (previously Venezuelan Environment Ministry) but ary, who then re-sold it to a Colombian buyer, this was re- law enforcement is carried out by the military and police, corded as both local and international trade.   with the Ministry playing a supporting role (Ojasti, ). We compiled , records of domestic and international  The country’s law on wildlife use has not changed since trade of psittacids, from five sources: ( ) national and inter-   (Congreso de la República de Venezuela, ) and, national enforcement agencies, ( ) the CITES trade data-   in general, wildlife use is permitted via special licenses, in- base, ( ) published and unpublished literature, ( ) internet  cluding for scientific sampling, pest control, and sport and social networks, and ( ) reports of donated and seized wild- commercial hunting. There is no distinction made between life from national zoos. subsistence hunting and sport hunting. Wildlife take without Data from the first three sources were compiled by  a permit is punishable by fines and up to  years in prison; Sánchez-Mercado et al. ( ). Data from national enforce-  possession is penalized by seizure of the animal (República ment agencies comprised reports of seized wildlife at the – de Venezuela, ). Venezuela ratified CITES in  and national level for , provided by the Venezuelan restricts exports of all native wildlife. Hunting of all psittacid Environment Ministry. According to Ministry personnel, species is banned, and the majority of psittacids are listed in in all cases their reports referred to national traders selling Appendix II of CITES, with three (Amazona barbadensis, goods on international markets, and the final destination of Ara macao and Ara militaris) listed in Appendix I specimens depended on the effectiveness and speed of re- (UNEP-WCMC, ). There are no captive-breeding or sponse of international dealers. If international dealers sustainable use programmes or government-sanctioned delay, national traders try to sell their goods in domestic management plans for psittacids in Venezuela (Bigio et al., markets before the animals sicken or die (A. Martínez,  ; Morales & Dessene, ). pers. comm.; Sánchez-Mercado et al., ). Thus, we categorized the Ministry’s records as domestic and international trade, to avoid underestimating international trade when the Study species trade was detected at the national level.  Although the number of taxa within the family Psittacidae is Data from national enforcement agencies comprised relatively stable, their classification is uncertain (Joseph records from the U.S. Fish and Wildlife Service of seized – et al., ). We used the taxonomy of the IUCN Red List wildlife from Venezuela during . CITES data  (IUCN, ), in which  psittacid species occurring in ( records) comprised wildlife and wildlife products – Venezuela are reported, from the genera Amazona (), seized from Venezuela during . Literature data  Pyrrhura (), Ara (), Pionus (), Touit (), Brotogeris (), ( records) were compiled from national and internation- Forpus (), Pyrilia (), Psittacara (), Aratinga (), al published and grey literature, from five online databases: Deroptyus (), Bolborhynchus (), Diopsittaca (), Eupsittula ISI Web of Knowledge, Scirus, JSTOR, Google Scholar, and (), Hapalopsittaca (), Nannopsittaca (), Orthopsittaca (), Zoological Record. We focused on ecology, conservation Pionites () and Thectocercus (), Thectocercus acuticaudatus, and anthropology journals, and used keywords in English previously classified as Aratinga acuticaudata; Remsen et al., and Spanish related to psittacid trade: Venezuela, poach, ). Four of these species are categorized as threatened hunt, harvest, trade, and traffic. We also consulted the web- (Supplementary Table S). site of TRAFFIC, the wildlife trade monitoring network

(TRAFFIC, ). To search the grey literature we requested and taxonomic biases in the data, this index cannot be inter- support from Red Ara Venezuela, a network of Venezuelan preted as an accurate estimate of offer, but as an index of environmental NGOs, to source internal reports and psitta- detectability (i.e. how frequently the sale of a given species cid trade records from NGOs, consulted the websites of na- is detected). We also calculated an extraction rate by species, tional ecology and ornithology conferences to find relevant as the number of specimens sold per year. abstracts, and asked wildlife managers and ornithologists To evaluate complementarity among sources, we summar- for information and for additional contacts who might ized the number of records and species obtained from each have information about psittacid trade. source according to type of trade (domestic or international). We asked the Venezuelan Association of Zoos and We also calculated Cohen’skappa(κ) as an index of inter- Aquariums for records of psittacids handed over by mem- source agreement in species detected (i.e. inter-source reliabil- bers of the public (former pets that were no longer wanted) ity), using the function kappa in package irr in Rv... or those confiscated by authorities and placed in zoos. (R Development Core Team, ). Cohen’skapparanges However, we received information for only two of the  from − to +,where represents the amount of agreement private and public zoos in Venezuela (Ministerio del that can be expected from random chance, and  represents Poder Popular para el Ambiente, ), Bararida Zoo in perfect agreement between the sources (McHugh, ). Barquisimeto and Metropolitan Zoo in Maracaibo, for To visualize temporal variation in the detection of psitta- which we obtained a total of  records for – cid trade, we plotted the accumulated number of records by (Supplementary Table S). year for the four most detected species. We also plotted the We monitored the activity of national Facebook groups accumulated number of records of domestic and inter- during January –May . Using the keywords wildlife national trade by year. sale, animal sale, bird sale, and aviary, we identified    groups ( public and closed), and we monitored the Results weekly activity of the  public groups. For each post we recorded the link, publication date, city of publication, type of Complementarity of sources post (offer or demand), number of specimens offered for sale, sex and development stage of specimens (adult, fledg- In total, we detected  species of psittacids traded in ling), and the price (and currency). Taxonomic identifica- Venezuela, of which  were non-native, apparently traded tion of species was based on images and the common from Africa, Central America, the Caribbean, USA and name and description provided in the post, using Hilty other South American countries (Supplementary Table S). () as a guide for morphological characteristics. When The most complete sources regarding number of species identification at species level was not possible we used broader detected were CITES and the zoos, accounting for  and  taxonomic categories (genus or family). We validated com- species, respectively (Table ). In general, agreement be- mon and scientific names (considering synonyms, alternative tween sources regarding the species detected was low spellings and subspecies) using the Encyclopedia of Life (κ , .), with the highest complementarity between the lit- (). We obtained  reports of parrot trade. erature and the Venezuelan Environment Ministry Within each of the above sources we considered a record (κ = .), followed by the literature, zoos and CITES as a single observation in time of a unique combination of (κ values .–.), and the Environment Ministry, the following information: () location, () observation date, Facebook, zoos and CITES (κ values .–.; Table ). () species involved, () sex and development stage, and () The sources with the lowest levels of complementarity quantity reported (number of specimens). with other sources were the zoos and CITES (Table ). Zoos were the only source reporting trade for Agapornis per- sonata, Amazona leucocephala, Aratinga jandaya, Aratinga Analysis leucophtalmus, Pionus chalcopterus, Pionus fuscus and We summarized the number of specimens recorded by Pyrrhura lepida. CITES was the only source reporting trade species (O ), and calculated a specific offer index (SO) for of Amazona aestiva, Amazona autumnalis, Brotogeris chry- i  each species based on how frequently it was offered for soptera and Psittacara mitratus (Supplementary Table S ). sale (Marín-Espinoza et al., ): In general, sources tend to focus on one type of trade, but literature review and the Environment Ministry provided re- =( / )×( / )× , SO Oi Ot m t 100 cords for both domestic and international trade (Table ).

where Oi is the number of sales of individuals of species i per year (i.e. number of records), Ot the total number of species Magnitude and scope of illegal trade traded illegally, m the number of years when species i was offered for sale, and t the total period of study (i.e.  The , records of illegal trade corresponded to , years, –). However, given the spatial, temporal specimens, with an overall extraction rate of ,

TABLE 1 The number of records of psittacids in the illegal trade in Venezuela, with the numbers of specimens and species recorded, from various sources. The number of records reporting domestic or international trade are also shown.

Source Number of records Number of specimens Number of species Domestic International Literature review 140 2,419 22 139 19 Venezuelan Environment Ministry 329 2,220 23 329 329 U.S. Fish & Wildlife Service 17 60 11 0 17 Facebook 167 258 25 160 2 Zoos 117 343 28 117 0 CITES 340 636,375 29 0 340 Total 1,110 641,675

TABLE 2 Inter-source reliability regarding the recording of psittacid species traded illegally in Venezuela, with Cohen’s kappa (κ) for each pair of sources.

Venezuelan Environment U.S. Fish & Wildlife Literature Ministry Service Facebook Zoo CITES Literature 1.000 0.259 −0.020 0.072 0.102 0.114 Venezuelan Environment 1.000 0.043 0.119 0.124 0.198 Ministry U.S. Fish & Wildlife Service 1.000 0.051 −0.090 −0.001 Facebook 1.000 0.034 −0.001 Zoo 1.000 0.015 CITES 1.000

individuals per year ( years of accumulated reports). (Fig. a). The number of records of A. ochrocephala in- Amazona ochrocephala was the most frequently detected creased sharply after , whereas there was a steady in- species (SO = .), with the highest extraction rate crease in the number of records of the other three most (, individuals per year). The second and third most fre- frequently detected species (Fig. b). quently detected species, E. pertinax and Amazona amazo-   nica, had similar frequencies of detection (SO = . and Discussion .); however, the number of A. amazonica individuals traded per year was almost  times higher (Supplementary The illegal trade of psittacids in Venezuela has been a long- Table S). Ara ararauna, A. barbadensis and A. chloropterus standing threat, with domestic and international trade span- were the fourth most frequently detected species ning  years and involving %( species) of the psittacid (SO = .–.), but the number of individuals of A. bar- species occurring in the country as well as  non-native spe- badensis traded was  times lower than the other two species. cies. The number of traded species reported here is lower Although the trade of F. passerinus and A. macao was detected than in previous reports (e.g.  species reported by less frequently than the other species, it involved at least as Desenne & Strahl, ), but our findings are based on reli- many individuals as of A. amazonica (c. .; Table ). able quantitative data and not only on qualitative expert as- The majority of species () were traded principally in sessments. Of the six species for which trade was reported the domestic market (. % of records were related to previously but did not occur in our data, five (Amazona domestic trade). Ten species were reported to be traded in mercenaria, Pionopsitta caica, Pionopsitta barrabandi, similar proportions in the domestic and international Pyrrhura hoematotis and Pyrrhura picta) were categorized markets (–% of records; A. amazonica, A. barbadensis, as low level of trade by Desenne & Strahl (), although Amazona dufresniana, A. chloropterus, A. macao, A. mili- the authors did not report the frequency of trade. The taris, Diopsittaca nobilis, Thectocercus acuticaudatus, other species that did not occur in our data but had a high Nannopsittaca panychlora and Pionus menstruus). A similar level of trade according to Desenne & Strahl ()wasTouit number of species were traded predominantly in the in- batavica. There are two probable explanations for this non- ternational market (. % of records; A. aestiva, Amazona detected trade: the frequency of trade is too low to be de- albifrons, A. autumnalis, Amazona bodini, A. ochrocephala, tected, or geographical biases in our data sources limit our A. ararauna, A. macao, Psittacara mitrata, Brotogeris chry- capacity to detect species with more restricted distributions. sopterus and Pionus tumultuosus; Table ). A systematic sampling covering ecosystems and bioregions In general, the number of records increased over time, throughout the country is needed to discern between these with international trade being the most frequently detected two possibilities.

(a) this is the most sought after species for the pet trade because 600 International trade Domestic trade of its ability to imitate the human voice (Desenne et al., ). Furthermore, evidence from Mexico, Peru, Bolivia 400 and Brazil indicates that the illegal parrot trade is largely domestic (Herrera & Hennessey, ; Gastañaga et al., ; Silva Regueira & Bernard, ).

No. of reports No. 200 Both the domestic and international illegal trade of psittacids in Venezuela are focused on widespread and 0 abundant species (A. ochrocephala, E. pertinax and A. amazonica), supporting the notion that the trade is opportunis- tic in nature (Silva Regueira & Bernard, ). Previous (b) A. ochrocephala  250 A. amazona studies have posited that at least species, including ma- E. pertinax caws (i.e. A. ararauna and A. chloropterus) and parakeets A. barbadensis 200 (i.e. T. acuticaudatus and E. pertinax), are subject to equiva- lent trade intensity (Gastañaga et al., ; Pires, ). The 150 frequency of trade in A. ochrocephala was seven times higher than for macaws, and the number of specimens traded 100 was – times higher. The effect of this extraction rate on

No. of reports No. the distribution range and population viability of A. ochro- 50 cephala requires evaluation. The species affected by international trade were not the 0 same as those affected by domestic trade. For international 1980 1985 1990 1995 2000 2005 2010 2015 markets, large parrots (five Amazona species), including the FIG. 1 Number of accumulated records of illegal psittacid trade widespread and common A. ochrocephala, and large main Venezuela by year (a) by type of trade and (b) by number of caws (two Ara species) are exported from Venezuela. This records of the four most frequently detected species. finding supports the notion that the most attractive species (large body size, colourful and with the ability to imitate human speech), such as amazons and macaws, are more As expected, each source complemented the figure for likely to be exported (Desenne & Strahl, ). Half of the the number of species involved in trade. The fact that na- species involved in international trade were not native to tional zoos accounted for % of detected species highlights Venezuela (e.g. A. albifrons, A. aestiva, P. mitratus and P. their importance in monitoring illegal wildlife trade. In tumultuosus), suggesting that Venezuela could be an im- Venezuela, as in other South American countries, zoos are portant transit country for the trade in parrot species offered animals by members of the public and are required from Central America and other South American countries. to receive animals confiscated by the authorities, and thus The domestic market was more focused on parakeets are an important source of information about domestic (Aratinga and Brotogeris spp.), small parrots (Pionus spp.) wildlife trade (Cuarón, ). and parrotlets (Forpus spp.). Species traded in both domes- Although we are confident in our estimation of the num- tic and international markets were mostly large parrots (in- ber of psittacid species traded, based on the accumulation of cluding the threatened A. barbadensis, and A. amazonica), reports over  years, our findings on the magnitude of trade large macaws (A. chloropterus and A. militaris) and small is clearly an underestimation. Quantitative assessments of parrots (Aratinga spp. and Pionus spp.). psittacid trade in Mexico (Cantú Guzmán et al., ) and Our approach of compiling and systematizing informa- Bolivia (Herrera & Hennessey, ) indicate that only tion about illegal trade in psittacids from various sources –% of parrot trade is detected by enforcement patrols. should be taken as the first step to develop a national mon- Underestimation of the magnitude of trade was evident in itoring programme to inform national policy on illegal wild- our various data sources: combined, records from the litera- life trade. The patterns and numbers provided could be used ture, zoos and seizures accounted for only , % of the num- to update the official list of threatened species in Venezuela, ber of specimens traded, whereas CITES data accounted for which currently includes four psittacids (A. barbadensis, T. %. This suggests that international trade is more import- acuticaudatus, A. militaris and Hapalopsittaca amazonina; ant than domestic trade (all CITES records were of inter- Rodríguez et al., ). This baseline information could national trade), but we suspect this result reflects the also be used to plan effective conservation actions, taking limited capacity of law enforcement at the national level ra- into account budget constraints and the limited infrastruc- ther than a real pattern. For example, barely % of records ture for wildlife-use monitoring and law enforcement of A. ochrocephala were detected at national level, although (Briceño-Linares et al., ).

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