The illegal pet trade is driving Madagascar's ploughshare tortoise to extinction

Page created by Wesley Molina
 
CONTINUE READING
The illegal pet trade is driving Madagascar's ploughshare tortoise to extinction
The illegal pet trade is driving Madagascar's
             ploughshare tortoise to extinction
                      ANGELO R. MANDIMBIHASINA, LANCE G. WOOLAVER, LIANNE E. CONCANNON
                                E. J. MILNER-GULLAND, RICHARD E. LEWIS, ANDREW M.R. TERRY
                               N I A R A H A F I L A Z A H A , L Y D I A L . R A B E T A F I K A and R I C H A R D P . Y O U N G

             Abstract The illegal wildlife trade is driving declines in                             Introduction
             populations of a number of large, charismatic animal
             species but also many lesser known and restricted-range
             species, some of which are now facing extinction as a
                                                                                                    I   llegal wildlife trade involves the collection, transporta-
                                                                                                        tion, and distribution of living or dead animals, animal
                                                                                                    parts and derivatives, both domestically and internationally,
             result. The ploughshare tortoise Astrochelys yniphora,
                                                                                                    in contravention of foreign and domestic laws and treaties
             endemic to the Baly Bay National Park of north-western
                                                                                                    (Wyler & Sheikh, ). It is a major and growing challenge
             Madagascar, is affected by poaching for the international
                                                                                                    for conservation. Although the global volume of illegal wild-
             illegal pet trade. To quantify this, we estimated population
                                                                                                    life trade is difficult to quantify (Rosen & Smith, ), its
             trends during –, using distance sampling sur-
                                                                                                    value is estimated at USD – billion per annum
             veys along line transects, and recorded national and
                                                                                                    (Lawson & Vines, ). Illegal trade is pushing many high-
             international confiscations of trafficked tortoises for
                                                                                                    profile species such as the tiger Panthera tigris, African
             –. The results suggest the ploughshare tortoise
                                                                                                    elephant Loxodonta africana, and white and black rhinocer-
             population declined . % during this period, to c. 
                                                                                                    oses Diceros bicornis and Ceratotherium simum, towards
             adults and subadults in –. Prior to  very
                                                                                                    extinction (Bennett, ; Biggs et al., ; Underwood
             few tortoises were seized either in Madagascar or inter-
                                                                                                    et al., ; TRAFFIC, ).
             nationally but confiscations increased sharply from .
                                                                                                         Illegal trade also affects a wide range of lesser-known spe-
             Since  poaching has intensified, with field reports sug-
                                                                                                    cies (Rosen & Smith, ) that often receive little inter-
             gesting that two of the four subpopulations are extinct,
                                                                                                    national attention. Reptiles, and chelonians in particular,
             leaving an unknown but almost certainly perilously low
                                                                                                    are trafficked in large numbers, accounting for  and
             number of adult tortoises in the wild. This study has pro-
                                                                                                    %, respectively, of total seizures of live animals recorded
             duced the first reliable population estimate of the plough-
                                                                                                    in TRAFFIC Bulletins during – (Rosen & Smith,
             share tortoise and shows that the species has declined
                                                                                                    ). Collection of reptiles for illegal trade is rarely sustain-
             rapidly because of poaching for the international pet
                                                                                                    able and causes declines in wild populations (Zhou & Jiang,
             trade. There is an urgent need for increased action both
                                                                                                    ; Natusch & Lyons, ; Nijman et al., ), with tur-
             in Madagascar and along international trade routes if
                                                                                                    tles and tortoises being affected heavily (Jenkins, ;
             the extinction of the ploughshare tortoise in the wild is
                                                                                                    Cheung & Dudgeon, ; Horne et al., ). Linked to
             to be prevented.
                                                                                                    traditional rites, beliefs, food preferences and medicinal
             Keywords Anti-poaching, Astrochelys yniphora, chelonian,                               uses, tortoises have been trafficked primarily into
             distance sampling, illegal wildlife trade, line transect sur-                          South-east and eastern Asia, with a high number of exports
             veys, ploughshare tortoise, population monitoring                                      originating from Africa (Jenkins, ; Nijman & Shepherd,
                                                                                                    , ).
                                                                                                         All four of Madagascar’s endemic tortoise species, the ra-
                                                                                                    diated tortoise Astrochelys radiata, ploughshare tortoise
             ANGELO MANDIMBIHASINA* (Corresponding author), LANCE WOOLAVER, RICHARD
                                                                                                    Astrochelys yniphora, spider tortoise Pyxis arachnoides and
             E. LEWIS and NIARAHA FILAZAHA Durrell Wildlife Conservation Trust, Lot IIY             flat-tailed tortoise Pyxis planicauda, are listed on Appendix
             49 J Ampasanimalo, BP 8511, 101 Antananarivo, Madagascar                               I of CITES () and categorized as Critically Endangered
             E-mail angelo.ramy@durrell.org
                                                                                                    on the IUCN Red List (Leuteritz et al., ; Leuteritz &
             LIANNE CONCANNON, ANDREW R. M. TERRY and RICHARD YOUNG Durrell Wildlife
             Conservation Trust, Trinity, Jersey, Channel Islands
                                                                                                    Pedrono, ; Leuteritz & Rioux Paquette, ;
                                                                                                    Leuteritz & Walker, ). All have been, or are currently,
             E. J. MILNER-GULLAND Department of Zoology, University of Oxford, Oxford, UK
                                                                                                    affected by illegal collection from the wild for the inter-
             LYDIA L. RABETAFIKA Department of Animal Biology, Faculty of Sciences,
             University of Antananarivo, Antananarivo, Madagascar
                                                                                                    national pet trade (O’Brien et al., ; Pedrono, ;
                                                                                                    Walker & Rafeliarisoa, ).
             *Also at: Department of Animal Biology, University of Antananarivo,
             Antananarivo, Madagascar                                                                    The ploughshare tortoise has long been considered one
             Received  September . Revision requested  November .                       of the world’s rarest tortoises (Juvik & Blanc, ; Curl
             Accepted  December . First published online  September .                     et al., ), perhaps in part because of a long history of

                                                                                        Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
The illegal pet trade is driving Madagascar's ploughshare tortoise to extinction
Illegal trade in ploughshare tortoises                 189

           exploitation. Vaillant & Grandidier () describe a naval                            the ploughshare’s active season during which breeding oc-
           archive from the th century which notes that stores in                               curs and the latter with a long period of low activity and
           the region were full of tortoises, many of which were pur-                             aestivation.
           chased by Arab sailors. Although historically ploughshare                                 Ploughshare tortoise habitat comprises dense patches
           tortoises were exploited for food, demand has shifted in                               of bamboo thicket Perrierbambus madagascariensis, scrub-
           the latter part of the th century to keeping them as pets,                           shrub, and palm savannah (Smith et al., a), with
           primarily in South-east Asia (Kiester et al., ; Raghavan                           bamboo thicket being the least accessible and most difficult
           et al., ). The ploughshare tortoise has been protected by                          to survey (Juvik et al., ). The suitable habitat patches are
           Malagasy law since  (the law was revised in ),                                 isolated, separated from each other by grass savannahs,
           which prohibits collection from the wild, transportation,                              seasonal rivers, lakes, mangroves, marshes, salt marshes
           keeping in captivity as pets, consumption, sale or export                              and the Bay of Baly (Fig. ). Two patches of habitat,
           of live individuals.                                                                   Cap Sada ( ha) and Beheta ( ha) are located on the
               Currently found only in the bamboo scrub habitats                                  eastern side of the bay and two, Betainalika (, ha) and
           around Baly Bay on the north-western coast of Madagascar,                              Ambatomainty (, ha), on the western side
           there is no evidence from the historical or sub-fossil record to                       (Mandimbihasina & Woolaver, ).
           suggest that the species was ever found outside of this highly
           restricted locality. All known ploughshare habitats are now
           legally protected as core zones of Baly Bay National Park                              Methods
           (Fig. ), established in . All entry, except for conservation
           and research purposes, is forbidden.                                                   Line transect population surveys and analyses
               A number of ploughshare tortoise population surveys
           have been carried out. In the mid s the population                                 Distance sampling (Buckland et al., ) is widely used for
           was estimated to be – individuals (Curl, ) and                               monitoring land tortoises (Swann et al., ; Leuteritz
           an estimate of  ±  individuals was reported in                               et al., ; Young et al., ; Smith et al., ; Walker
           (Pedrono, ). The survey methods used to produce                                    & Rafeliarisoa, ) and has been carried out by Durrell
           these estimates did not account for biases arising from                                Wildlife Conservation Trust periodically since  (with
           imperfect detection, nor did they cover the species’ full                              a pilot study in –) to estimate ploughshare tortoise
           range; consequently there is no reliable information on                                densities. Line transects were surveyed in October–April in
           historical or current population sizes.                                                –, – and –, between .–.
               A significant decline in numbers of the ploughshare tor-                           and .–., because tortoises were more active during
           toise is suspected to have occurred during –, but                              these cooler hours. For a given transect, a team of – sur-
           this has not been quantified. Here we present the results                              veyors walked in parallel lines  m apart, with a team leader
           of surveys conducted during – covering the entire                              in the middle responsible for navigating and measuring the
           species range, with the first robust estimates of ploughshare                          length of the transect. The survey team consisted of a pro-
           tortoise population size and trend. We report data from                                fessional biologist acting as team leader and trained mem-
           anti-poaching patrols conducted since  to understand                               bers of the local community. All team members walked
           more recent population changes and also examine data                                   along the line transect at the same speed of .–. km/h
           from seizures of ploughshare tortoises over the same                                   and in the same direction (either east–west or north–
           -year period as an indicator of the level of trafficking of                          south). The leader and the surveyors at the ends of the
           this species.                                                                          line used global positioning system (GPS) units to record
                                                                                                  the travel distance and ensure the walked lines were as
                                                                                                  straight as possible. The transect length was then calculated
           Study area                                                                             as the distance walked by the survey team multiplied by the
                                                                                                  number of people in that team.
           We carried out line transect surveys at Ambatomainty,                                      For each survey session .–. km long line transects
           Betainalika, Beheta and Cap Sada, the four known sites sup-                            were randomly placed at least  m apart to cover all four
           porting extant ploughshare tortoise subpopulations within                              sites of ploughshare tortoise habitat. One area of c.  km
           the Baly Bay National Park (Fig. ). There is also a reintro-                          in the centre of the largest site of tortoise habitat in
           duction site at Beaboaly, where a known number of released                             Ambatomainty was too difficult to access and remained
           tortoises are intensively monitored. The Park is located                               unsampled. Eighty-eight transects with a total length of
           around Baly Bay in the Region of Boeny on the north-                                   . km were surveyed in –, . km ( trans-
           western coast of Madagascar. This region has two distinct                              ects) in –, and . km ( transects) in –.
           seasons: a rainy, hot period December–March, and a dry,                                    When a tortoise was found, all observers stopped survey-
           cooler season April–November. The former coincides with                                ing while data were recorded. The perpendicular distance

           Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
190         A. Mandimbihasina et al.

             FIG. 1 Map of Baly Bay National Park, Madagascar, showing the strict conservation zones of the National Park and sites of suitable
             habitat for ploughshare tortoises Astrochelys yniphora. The Ambatomainty, Beheta, Betainalika and Cap Sada sites were surveyed in
             three survey periods: –, – and –.

             from the tortoise to the line of the surveyor that found it was                        activity (e.g. illegal camps, campfires, paths) and recording
             measured. Sex of adults (based on plastron curvature and                               numbers and locations of any ploughshare tortoises seen.
             anal fork opening), identification number of previously                                Patrol teams carried GPS units to measure distances walked
             marked animals, and body measurements were recorded                                    and recorded start and finish times of their daily patrols.
             for each tortoise. Individuals were assigned to one of two                             We calculated the effort (distance walked and time spent
             age categories based on their size: adult or subadult if they                          patrolling) of the anti-poaching patrols conducted during
             had a carapace length .  cm, and juvenile if ,  cm.                                January –May  and the encounter rates (tortoises
             It was not possible to distinguish between the sexes of juve-                          encountered per km walked). Data analyses were carried
             niles during field surveys because this is only possible with                          out using Distance v. . (Thomas et al., ).
             endoscopy.                                                                                 Although population size was estimated at the subpopu-
                 The accuracy of this transect methodology was tested                               lation level, here we report global population estimates to
             during a pilot study in Cap Sada in –. Cap Sada                                avoid providing traffickers with information about tortoise
             is the best studied of the wild subpopulations of the plough-                          numbers at each site that could influence poaching. For
             share tortoise, with research carried out at this site since the                       both the Cap Sada pilot study and the wider survey the
             s (e.g. Juvik & Blanc, ; Juvik et al., ; Smith et al.,                     data were truncated to exclude the % of distances furthest
             b). Nearly all adult and subadult tortoises in Cap Sada                            from the transect line, to discard unusual observations
             had been permanently marked by  and their total num-                               (Thomas et al., ). Based on lowest Akaike Information
             ber was known. Twenty-seven transects with a total length                              Criterion (AIC) values and visual inspection of the detection
             of . km, arranged in a systematic grid to ensure good                               functions, we selected the half-normal cosine model for
             coverage of the entire area of suitable habitat, were surveyed                         density estimation in both cases.
             in – and the results were compared to the known
             population size of adults in the subpopulation.
                 In an attempt to understand the status of the ploughshare                          National and international confiscation data
             tortoise population since , we collated data on any tor-
             toises observed in the wild during anti-poaching patrols                               We collated records of ploughshare tortoises seized by
             conducted in Baly Bay National Park. The patrols covered                               authorities outside Madagascar as reported in TRAFFIC
             the sites of all four wild subpopulations and the reintro-                             Bulletins from June –December  (TRAFFIC,
             duced subpopulation, searching for signs of poaching                                   ), and accessed from the TRAFFIC website. The age

                                                                                        Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
Illegal trade in ploughshare tortoises                 191

           of seized tortoises was not always reported, so we recorded                            ploughshare tortoises between – and –,
           only the number of individuals confiscated. Numbers of                                 and a negligible difference between – and –
           juveniles and adults were known for all confiscations in                               . The overall decline in the mean population estimates
           Madagascar, so these were used to explore which age classes                            over the -year period is %.
           were most targeted by poachers. We also collated all avail-                               However, reports from anti-poaching patrols and con-
           able anecdotal and reported evidence of trafficking, sales                             servation NGO field teams during January –May 
           and demand, to examine the dynamics of illegal trade of                                suggest the situation has deteriorated further. Multiple visits
           ploughshare tortoises.                                                                 by both groups during this period covered all four main sites
                                                                                                  of suitable habitat, plus the reintroduction site, in both the
                                                                                                  active and low activity seasons. Quality-controlled data of
           Results                                                                                patrol effort were only available for Beaboaly, where the
                                                                                                  joint anti-poaching teams conducted , hours of patrol-
           Tortoise population trends                                                             ling covering , km to protect the reintroduced popula-
                                                                                                  tion. For the other four sub-populations, patrols totalled
           In our Cap Sada pilot study in – we observed                                 , hours. This at least equals the effort (in terms of
           adults along  transect lines totalling . km. Despite                              time spent searching for tortoises and surface area covered)
           the small sample size, the detection function provided a                               of conducting the , km of surveys during –.
           good fit to the data (χ = ., P = .) and we estimated                            Despite this large-scale and intensive search effort, no ani-
           a density of . adult tortoises per ha (% CI = .–.                           mals have been seen in two of the wild subpopulations since
           adult tortoises per ha) and a population size of  indivi-                            the end of . The situation is less clear for the other two
           duals (% CI = – tortoises). This is relatively close                             subpopulations, but given the low encounter rates that were
           to the  adults believed to be in the subpopulation at the                            observed, we suspect that both have been severely depleted
           time based on data from the long-term mark-recapture                                   since  and (based on only one individual being found)
           study (Smith et al., b) of –.                                              one subpopulation now consists of ,  individuals.
              Despite a survey effort of .  km per survey session,
           totalling . km of line transects over the -year moni-
           toring period, we did not meet the target number of tortoise                           Trends in confiscations
           observations required (– data points per period;
           Buckland et al., ) to reliably model a detection function                          The first report of ploughshare tortoises confiscated outside
           for each of the three sampling periods. Therefore the data                             Madagascar was of three individuals seized in Belgium
           were pooled to estimate a global detection function (i.e. ap-                          in . The next was one individual confiscated in Japan
           plied to all three survey periods; Obbard et al., ), which                         in . The number seized per year outside Madagascar
           showed no signs of avoidance of the survey line or heaping                             has increased since  (Fig. ) with peaks in  ( tor-
           of observations at any distance, which was post-stratified to                          toises) and  (). A total of  ploughshare tortoises
           generate population abundance and density estimates for                                have been confiscated outside Madagascar in  separate
           each survey period. The detection function provided a                                  seizures during – (Fig. ).
           good fit to the data (χ = ., df = , P = .), and was                             The first confiscation recorded in Madagascar was in
           used to estimate density because it had the lowest AIC                                 , of nine adults in a single seizure, and only a single
           value across all possible models.                                                      juvenile was confiscated during the following -year period
              Ploughshare tortoise encounter rates and population                                 up to . However, since  the number of confiscated
           density and size estimates for each survey session are                                 ploughshare tortoises in Madagascar has increased each
           presented in Table . The confidence intervals around the                              year (Fig. ) with peaks in  ( tortoises) and 
           mean estimated population sizes are large, but the difference                          (). The total number of ploughshare tortoises confiscated
           in the mean estimates suggest a rapid decline in wild                                  within Madagascar during – was  individuals

           TABLE 1 Number of ploughshare tortoises recorded (A, adults; SA, subadults; J, juveniles) during surveys, encounter rates, and population
           density and size estimates with lower and upper % confidence limits (CL).

                              Distance              Tortoises recorded        Encounter rate A + SA/J Density                            Population       Lower         Upper
           Time period        surveyed (km)         A + SA/J                  (tortoises per km)      (tortoises per ha)*                size*            95% CL        95% CL
           2006–2008          563.9                 43/15                     0.076/0.027                      0.076                     1,105            709           1,722
           2011–2013          514.2                 26/18                     0.056/0.035                      0.036                       517            174           1,535
           2014–2015          552.1                 38/13                     0.067/0.024                      0.035                       506            188           1,359
           *Population density and size estimates are for adults and subadults only.

           Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
192         A. Mandimbihasina et al.

                                                                                                                                            FIG. 2 Number of ploughshare
                                                                                                                                            tortoises confiscated
                                                                                                                                            internationally and in
                                                                                                                                            Madagascar in –
                                                                                                                                            (age-specific data were only
                                                                                                                                            available for national
                                                                                                                                            confiscations). Numbers above
                                                                                                                                            each column indicate number of
                                                                                                                                            seizures (international/
                                                                                                                                            Madagascar) for that year.
                                                                                                                                            Juveniles were defined as tortoises
                                                                                                                                            with a carapace length ,  cm.

             ( adults and  juveniles) in  seizures. The total num-                           pers. comm.). Nine of these were confirmed as having re-
             ber of seizures (international and national) was highest in                            cently been taken from wild populations, based on identifi-
             – (, ,  seizures, respectively) and  (), com-                        cation markings visible in the online photographs.
             pared with – seizures in all other years.

                                                                                                    Discussion
             Additional evidence of illegal wildlife trade
                                                                                                    Our study provides the first estimates of ploughshare tor-
             During the period of rapid population decline, NGO field                               toise population size and trend based on range-wide sur-
             teams in Baly Bay observed an escalation in the reported                               veys, using a method that takes imperfect detection into
             price being offered to local poachers by collectors for an                             account. Our results reveal that the ploughshare tortoise
             adult ploughshare tortoise, from c. USD  in , to                                  probably declined by . % during –, but more re-
             USD  in  and USD  in  (Jinoro Delphin,                                    cent field patrols suggest an even larger decline, with some
             pers. comm.). For context, the mean local wage in the                                  subpopulations (at least the adults and subadults) now
             villages adjacent to the National Park is USD .– per day                            probably extinct. Concurrent data on escalating confisca-
             (Andrianandrasana, ).                                                              tions in Madagascar and South-east Asia, together with
                 The main intended destinations for ploughshare tor-                                anecdotal evidence of high and increasing levels of poaching
             toises, based on confiscation patterns, are Thailand,                                  activity in Baly Bay, identify the illegal international pet
             Malaysia, Singapore, Indonesia and Hong Kong, with                                     trade as the driver of this rapid and severe decline.
             animals transiting through Kenya and Abu Dhabi from                                        Given the low population density of this species, over
             Madagascar (TRAFFIC, ). Although data are lacking                                  , km of survey effort was required to obtain sufficient
             on trade routes into China, it is suspected that many traf-                            sample sizes for analyses. The remoteness and relative in-
             ficked animals are destined for collectors there (Gibbons,                             accessibility of the study area, combined with the cryptic na-
             ). Collectors in demand countries pay high prices for                              ture of the species and its short active season, resulted in
             ploughshare tortoises, with recent reports of tortoises for                            several limitations of the survey. Firstly, because of lower
             sale in Indonesia from USD  for a small individual to                               than anticipated numbers of tortoise detections, our popu-
             USD , for a large animal (Morgan & Chng, ).                                   lation estimates had relatively wide confidence intervals (al-
                 Use of the internet and social media platforms appears to                          though our pilot study of the line transect method to survey
             facilitate illegal trade of ploughshare tortoises (Morgan &                            the Cap Sada population produced a population estimate
             Chng, ), which first started appearing for sale online                             close to the known population size, despite the low numbers
             in c.  (Walker, ; Kiester et al., ). We suspect                            of observations). Secondly, we were not able to access the
             there has been a recent spike in online sales, e.g. five adult                         central portion of Ambatomainty, the western-most and lar-
             ploughshare tortoises were on sale on a Hong Kong website                              gest patch of suitable habitat, because of its remoteness and
             in , and seven were for sale online in  (R. Lewis,                             dense vegetation. In the analysis, we assumed tortoise

                                                                                        Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
Illegal trade in ploughshare tortoises                 193

                                                                                                      Despite these limitations, we believe the evidence pre-
                                                                                                  sented here points to a catastrophic decline in the plough-
                                                                                                  share tortoise. In – the estimated density of
                                                                                                  individuals of or near breeding age was only . individuals
                                                                                                  per km. To put this into context, the density (of all age
                                                                                                  classes) of the rare and threatened Sonoran desert tortoise
                                                                                                  Gopherus agassizii at an arid mountain site in the southern
                                                                                                  USA was  individuals per km (Zylstra et al., ). The
                                                                                                  lack of ploughshare tortoise observations since January
                                                                                                  , despite repeated field visits, leads us to suspect that
                                                                                                  only one of the four wild subpopulations contains . 
                                                                                                  adults and subadults, and two of the subpopulations have
                                                                                                  probably been extirpated. Given its long generation time
                                                                                                  of c.  years and limited capacity to recover from popula-
                                                                                                  tion declines, this species is now in a perilous situation and
                                                                                                  its survival is at risk.
                                                                                                      At the time of writing,  ploughshare tortoises have
                                                                                                  been confiscated (both within and outside Madagascar)
                                                                                                  during trafficking attempts since ,  of these since
                                                                                                  . Seizure data consistently and substantially underesti-
                                                                                                  mate actual numbers of animals poached (D’Cruze &
                                                                                                  Macdonald, ), and therefore the numbers of adults
                                                                                                  and juveniles taken from the wild and trafficked since
                                                                                                   may be in the low thousands (probably mostly juve-
                                                                                                  niles, which are not represented in our population esti-
                                                                                                  mates). Although it is not possible to evaluate temporal
                                                                                                  trends in enforcement effort, there has been an increase in
                                                                                                  corruption in Madagascar since the political instability
                                                                                                  commencing in , leading to a reduced capacity to con-
           FIG. 3 Photos of the illegal trade in ploughshare tortoises. (a) A                     trol illegal trade (Randriamalala & Liu, ; Gore et al.,
           shipment confiscated in Madagascar at Ivato International                              ). This corresponds with our survey results, which
           Airport in July  included  juvenile and  adult ploughshare                      show a significant drop in numbers between the first and
           tortoise,  radiated tortoises Astrochelys radiata, and a spider                     second survey periods, indicating that intensive poaching
           tortoise Pyxis arachnoides (Durrell Wildlife Conservation Trust,
                                                                                                  started c. .
           ). (b) A seizure of Malagasy tortoises in Thailand in 
           included  ploughshare tortoises and  radiated tortoises
                                                                                                      When the ploughshare tortoise population rapidly de-
           (Panjit Tansome, TRAFFIC ). (c) Five adult ploughshare                             clined, increasing effort will have been required by poachers
           tortoises, two of which are clearly engraved, for sale on a                            to locate tortoises in the wild, which could be a disincentive
           Chinese website in June .                                                          for poaching. However, the Anthropogenic Allee effect pre-
                                                                                                  dicts that increasing species rarity drives up desirability,
           density in this area to be equivalent to the mean density                              which in turn drives up the amount people are willing
           across the rest of the species’ range. Given its challenging ac-                       to pay (Hall et al., ; Lyons & Natusch, ). This is
           cessibility, this may be an important site for ploughshare                             reflected in the -fold increase since  in the local
           tortoises and requires continued intensive protection.                                 price paid to poachers for tortoises taken from the wild.
           Thirdly, as a result of the low numbers of juveniles observed,                         Given that ploughshare tortoises have been for sale for near-
           we were limited to estimating population size and density                              ly USD , in a demand country we anticipate that these
           for adults and subadults. Smaller individuals are hard to                              local price escalations may continue, sustaining the poach-
           detect in the dense bamboo scrub, but the lack of sightings                            ing intensity even as the global wild population of the
           of juveniles in some subpopulations in – and –                             ploughshare tortoise declines to just a few individuals.
           , compared with earlier years, suggests a decline in the                               Prior to the recent increase in poaching, the ploughshare
           number of individuals in this age class. Most of the plough-                           tortoise conservation programme had made good progress
           share tortoises confiscated have been juveniles, which can be                          towards achieving its goals, with successful habitat protec-
           more easily concealed and transported in large numbers                                 tion, reduction of threats from fire and cattle encroachment,
           (Fig. ), and this could partially explain the lack of sightings                       and a promising reintroduction programme (Durbin et al.,
           of juveniles.                                                                          ; Wallis, ; Mandimbihasina & Woolaver, ).

           Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
194         A. Mandimbihasina et al.

             However, the upsurge in international demand, facilitated                              field assistants. Funding for field surveys was provided by the Durrell
             by weakening governance and limited law enforcement,                                   Wildlife Conservation Trust, Disney Conservation Fund, Turtle
                                                                                                    Conservation Fund (2013 & 2014), Turtle Conservancy, and the U.S.
             resulted in conservation agencies having to adapt and diver-
                                                                                                    Fish & Wildlife Service’s Wildlife Without Borders (EA-0055/2009,
             sify their responses rapidly, to include anti-poaching                                 EA-0205/2011)—Critically Endangered Animals Conservation Fund.
             actions, judicial capacity development and national and
             international advocacy. It is clear that these interventions
             have not been sufficient in scale or intensity to reduce                               Author contributions Data collection, data analysis and writing of
             poaching. Even engraving the carapaces of all wild, released                           first draft: AM; help with fieldwork: NF; coordination of field research:
                                                                                                    LW, REL, LLR; compilation of confiscation data: LW, AM; assistance
             and captive ploughshare tortoises (John & Shepherd, )                              with data analysis: LC and RY; assistance with writing and editing: LW,
             appears to have failed to reduce demand, with engraved an-                             LC, EJMG, REL, AT; design lead of field research, writing and editing
             imals now for sale online. A lack of enforcement action                                of later drafts: RY.
             against traders or buyers of these engraved tortoises has
             probably contributed to the lack of success of this campaign.
                 Immediate action is needed to safeguard the remaining                              Conflicts of interest None.
             wild, released and captive populations. Anti-poaching ac-
             tions in Baly Bay must be scaled up and improved, including
                                                                                                    Ethical standards The research was authorized by Madagascar
             better detection of poachers (e.g. using patrol dogs), tortoise
                                                                                                    National Parks, the manager of Baly Bay National Park, and the
             protection (e.g. fences), and rapid response enforcement                               Ministry of Ecology, Environment and Forest of Madagascar during
             techniques that have been developed elsewhere to combat                                2006–2015. No specimen was taken from the wild during fieldwork; tor-
             poaching (Moreto & Lemieux, ; O’Donoghue & Rutz,                                   toises were only captured and handled for data recording during surveys.
             ; Avery, ). Captive populations are being estab-
             lished outside Madagascar as assurance colonies, using
             internationally confiscated animals (Kiester et al., ),                            References
             and new breeding centres are also required in Madagascar,
                                                                                                    A N D R I A N A N D R A S A N A , H. () Testing the effectiveness of
             with high-security measures to prevent animals being
                                                                                                        community-based conservation in conserving biodiversity, protecting
             stolen. Strategies to reduce the demand for wild animals                                   ecosystem services, and improving human well-being in Madagascar.
             should also be considered to secure the long-term future                                   DPhil thesis, University of Oxford, Oxford, UK.
             of the species. Demand reduction initiatives for other                                 A V E R Y , J. () Anti-poaching pooches. Man’s best friend plays a vital
             species, particularly in South-east and East Asia, have had                                role in the war against poaching. Africa Geographic Magazine, .
                                                                                                        Http://magazine.africageographic.com/weekly/issue-/
             limited success (Challender & MacMillan, ), with little
                                                                                                        anti-poaching-pooches/ [accessed  June ].
             evidence of effectiveness (Olmedo et al., ). The consu-                            B E N N E T T , E.L. () Another inconvenient truth: the failure of
             mers driving the trade in this species and other rare reptiles                             enforcement systems to save charismatic species. Oryx, , –.
             are a relatively small number of dealers and hobbyists, pre-                           B I G G S , D., C O U R C H A M P , F., M A R T I N , R. & P O S S I N G H A M , H.P. ()
             dominantly in eastern Asia, who seek out the rarest animals                                Legal trade of Africa’s rhino horns. Science, , –.
             and for whom the illegality of owning the species appears                              B U C K L A N D , S.T., A N D E R S O N , D.R., B U R N H A M , K.P., L A A K E , J.L.,
                                                                                                        B O R C H E R S , D.L. & T H O M A S , L. () Introduction to Distance
             not to be a deterrent. More research is required to under-                                 Sampling: Estimating Abundance of Biological Populations. Oxford
             stand the psychology of collectors and to identify the mes-                                University Press, Oxford, UK.
             saging to which this group would be responsive (Veríssimo                              C H A L L E N D E R , D.W.S. & M AC M I L L A N , D.C. () Poaching is more
             et al., ; Hinsley et al., ).                                                       than an enforcement problem. Conservation Letters, , –.
                 We conclude that the extinction of the ploughshare tor-                            C H E U N G , S.N. & D U D G E O N , D. () Quantifying the Asian turtle
                                                                                                        crisis: market surveys in southern China, –. Aquatic
             toise in the wild is imminent unless poaching for the illegal                              Conservation: Marine and Freshwater Ecosystems, , –.
             pet trade is halted. Even if poaching ceases, we suspect that,                         CITES () Convention on International Trade in Endangered
             given the extent of the demographic collapse of this species,                              Species of Wild Fauna and Flora. Appendices I, II and III. Http://
             its recovery is unlikely to happen without intensive manage-                               cites.org/eng/app/appendices.php [accessed  March ].
             ment such as large-scale reintroductions, and that even with                           C U R L , D.A. () The rarest tortoise on earth. Oryx, , –.
                                                                                                    C U R L , D.A., S C O O N E S , I.C., G U Y , M.K. & R A KO T O A R I S O A , G. ()
             such actions recovery is likely to take decades.
                                                                                                        The Madagascar tortoise Geochelone yniphora: current status and
                                                                                                        distribution. Biological Conservation, , –.
                                                                                                    D’C R U Z E , N. & M AC D O N A L D , D.W. () A review of global trends
             Acknowledgements We thank Madagascar National Parks and                                    in CITES live wildlife confiscations. Nature Conservation, , –.
             Madagascar’s Ministry of Ecology, Environment, Forest and Oceans                       D U R B I N , J., R A J A F E T R A , V., R E I D , D. & R A Z A N D R I Z A N A K A N I R I N A , D.
             for providing permits and the mandate to carry out this research within                    () Local people and project Angonoka – Conservation of
             Baly Bay National Park. The University of Oxford’s Biodiversity                            the ploughshare tortoise in north-western Madagascar. Oryx, ,
             Fellows Programme supported AM to analyse and write up the                                 –.
             work. We thank those that have helped with the field surveys including                 G I B B O N S , P. () Ploughshare Tortoise Trafficking Update. Turtle
             local villager patrol members, Baly Bay National Park staff, and local                     Conservancy, Ojai, USA. Https://www.turtleconservancy.org/news/

                                                                                        Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
Illegal trade in ploughshare tortoises                     195

               /ploughshare-tortoise-trafficking-update [accessed  March                             N AT U S C H , J.D. & L YO N S , J.A. () Exploited for pets: the harvest and
               ].                                                                                         trade of amphibians and reptiles from Indonesian New Guinea.
           G O R E , M.L., R AT S I M B A Z A F Y , J. & L U T E , M.L. () Rethinking                     Biodiversity and Conservation, , –.
               corruption in conservation crime: insights from Madagascar.                                 N I J M A N , V. & S H E P H E R D , C.R. () Trade in non-native,
               Conservation Letters, , –.                                                              CITES-listed, wildlife in Asia, as exemplified by the trade in
           H A L L , R.J., M I L N E R -G U L L A N D , E.J. & C O U R C H A M P , F. ()                  freshwater turtles and tortoises (Chelonidae) in Thailand.
               Endangering the endangered: the effect of perceived rarity on                                  Contributions to Zoology, , –.
               species extinction. Conservation Letters, , –.                                         N I J M A N , V. & S H E P H E R D , C.R. () Analysis of a decade of trade of
           H I N S L E Y , A., L E E , T.E., H A R R I S O N , J.R. & R O B E R T S , D.L. ()             tortoises and freshwater turtles in Bangkok, Thailand. Biodiversity
               Estimating the extent and structure of trade in horticultural orchids                          and Conservation, , –.
               via social media. Conservation Biology, , –.                                      N I J M A N , V., S H E P H E R D , C.R., M U M P U N I , S A U N D E R S , K.L. ().
           H O R N E , B.D., P O O L E , C.M. & W A L D E , A.D. () Conservation of                       Over-exploitation and illegal trade of reptiles in Indonesia.
               Asian tortoises and freshwater turtles: setting priorities for the next                        Herpetological Journal, , –.
               ten years. Recommendations and Conclusions from the Workshop in                             O B B A R D , M.E., S TA P L E T O N , S., M I D D E L , K.R., T H I B A U LT , I.,
               Singapore, February –, . Wildlife Conservation Society,                                B R O D E U R , V. & J U T R A S , C. () Estimating the abundance of the
               Singapore.                                                                                     Southern Hudson Bay polar bear subpopulation with aerial surveys.
           J E N K I N S , M.D. () Tortoises and Freshwater Turtles: The Trade in                         Polar Biology, , –.
               Southeast Asia. TRAFFIC International, Cambridge, UK.                                       O’B R I E N , S., et al. () Decline of the Madagascar radiated tortoise
           JUVIK, J.O., A N D R I A N A R I V O , A.J. & B L A N C , C.P. () The ecology and              Geochelone radiata due to overexploitation. Oryx, , –.
               status of Geochelone yniphora: A critically endangered tortoise in                          O’D O N O G H U E , P. & R U T Z , C. () Real-time anti-poaching tags
               northwestern Madagascar. Biological Conservation, , –.                                 could help prevent imminent species extinctions. Journal of Applied
           J U V I K , J.O. & B L A N C , C.P. () The Angonoka of Cape Sada.                              Ecology, , –.
               Animals, , –.                                                                       O L M E D O , A., S H A R I F , V. & M I L N E R -G U L L A N D , E.J. () Evaluating
           K I E S T E R , A.R., M A N D I M B I H A S I N A , A.R., L E W I S , R.E., G O O D E , E.V.,      the design of behaviour change interventions: A case study of rhino
               J U V I K , J.O., Y O U N G , R. & B L A N C K , T. () Conservation of the                 horn in Viet Nam. Conservation Letters, , –.
               Angonoka (Ploughshare tortoise) Astrochelys yniphora. Chelonian                             P E D R O N O , M. () Gestion interactive entre les populations sauvages
               Research Monographs, , –.                                                               et captives: Stratégie de conservation de la tortue Astrochelys
           L AW S O N , K. & V I N E S , A. () Global Impact of the IWT – The Costs                       yniphora à Madagascar. PhD thesis, Université Pierre et Marie
               of Crime, Insecurity and Institutional Erosion. Chatham House,                                 Curie, Paris, France.
               London, UK.                                                                                 P E D R O N O , M. () The Tortoises and Turtles of Madagascar. Natural
           L E U T E R I T Z , T. & P E D R O N O , M. (Madagascar Tortoise and Freshwater                    History Publications, Borneo.
               Turtle Red List Workshop) () Astrochelys yniphora. The IUCN                             R A G H AVA N , R., L U Z , S., S H E P H E R D , C.R., L E W I S , R., G I B B O N S , P. &
               Red List of Threatened Species . Http://dx.doi.org/./                                G O O D E , E. () A case study of the ploughshare tortoise and
               IUCN.UK..RLTS.TA.en.                                                           the role zoos can play in conservation. TRAFFIC Bulletin, ,
           L E U T E R I T Z , T. & R I O U X P A Q U E T T E , S. (Madagascar Tortoise and                   –.
               Freshwater Turtle Red List Workshop) () Astrochelys radiata.                            R A N D R I A M A L A L A , H. & L I U , Z. () Rosewood of Madagascar:
               The IUCN Red List of Threatened Species. Http://dx.doi.org/./                            between democracy and conservation. Madagascar Conservation &
               IUCN.UK..RLTS.TA.en.                                                           Development, , –.
           L E U T E R I T Z , T. & W A L K E R , R. () Pyxis arachnoides. The IUCN Red                R O S E N , G.E. & S M I T H , K.F. () Summarizing the evidence on the
               List of Threatened Species. Http://dx.doi.org/./IUCN.UK.                                 international trade in illegal wildlife. EcoHealth, , –.
               -.RLTS.TA.en.                                                             S M I T H , L.L., B O U R O U , R., M A H AT O LY , J. & S I B O , C. (a) Home
           L E U T E R I T Z , T., R A N D R I A M A H A Z O , H. & L E W I S , R. (Madagascar                range and microhabitat use in the Angonoka (Geochelone yniphora)
               Tortoise and Freshwater Turtle Red List Workshop) ()                                       in Madagascar. Chelonian Conservation and Biology, , –.
               Pyxis planicauda. The IUCN Red List of Threatened Species. Http://                          S M I T H , L.L., L I N E H A N , J.M., S T O B E R , J.M., E L L I OT T , M.J. & J E N S E N ,
               dx.doi.org/./IUCN.UK..RLTS.TA.en.                                        J.B. () An evaluation of distance sampling for large-scale
           L E U T E R I T Z , T.E.J., L A M B , T. & L I M B E R A Z A , J.C. (). Distribution,          gopher tortoise surveys in Georgia, USA. Applied Herpetology, ,
               status, and conservation of radiated tortoises (Geochelone radiata)                            –.
               in Madagascar. Biological Conservation, , –.                                       S M I T H , L.L., R E I D , D., B O U R O U , R., M A H AT O LY , J. & S I B O , C. (b)
           L Y O N S , J.A. & N AT U S C H , J.D. () Effects of consumer preferences                      Status and distribution of the angonoka tortoise (Geochelone
               for rarity on the harvest of wild populations within a species.                                yniphora) of western Madagascar. Biological Conservation, ,
               Ecological Economics, , –.                                                             –.
           M A N D I M B I H A S I N A , A. & W O O L AV E R , L. () The ploughshare                   S WA N N , D.E., A V E R I L L -M U R R A Y , R.C. & S C H WA L B E , C.R. ()
               tortoise Astrochelys yniphora. In Western Indian Ocean                                         Distance sampling for Sonoran desert tortoises. Journal of Wildlife
               Tortoises Ecology: Diversity, Evolution, Conservation,                                         Management, , –.
               Paleontology (ed. J. Gerlach), pp. –. Siri Scientific Press,                          T H O M A S , L., B U C K L A N D , S.T., R E X S TA D , E.A., L A A K E , J.L.,
               Manchester, UK.                                                                                S T R I N D B E R G , S., H E D L E Y , S.L. et al. () Distance software: design
           M O R E T O , W.D. & L E M I E U X , A.M. () Poaching in Uganda:                               and analysis of distance sampling surveys for estimating population
               perspectives of law enforcement rangers. Deviant Behavior, ,                                 size. Journal of Applied Ecology, , –.
               –.                                                                                    TRAFFIC () Seizures and prosecutions. TRAFFIC Bulletin,  ()
           M O R G A N , J., & C H N G , S. (). Rising internet-based trade in the                        (March )– () (October ).
               Critically Endangered ploughshare tortoise Astrochelys yniphora in                          TRAFFIC () TRAFFIC’s engagement on African rhinoceros
               Indonesia highlights need for improved enforcement of CITES.                                   conservation and the global trade in rhinoceros horn. Http://www.
               Oryx, https://doi.org/./SX.                                               traffic.org/rhinos/ [accessed  November ].

           Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
196         A. Mandimbihasina et al.

             U N D E R W O O D , F.M., B U R N , R.W. & M I L L I K E N , T. () Dissecting the      W A L L I S , D. (). Evaluating the short-term success of a
                illegal ivory trade: an analysis of ivory seizures data. PLoS ONE, ,                      reintroduction of the Critically Endangered ploughshare tortoise,
                e.                                                                                    Astrochelys yniphora. MSc thesis, Imperial College London,
             V A I L L A N T , L. & G R A N D I D I E R , G. () Histoire Naturelle des                 London, UK.
                Reptiles, Première Partie: Crocodiles et Tortues. In Histoire                           W Y L E R , L.S. & S H E I K H , P.A. () International Illegal Trade in
                Physique Naturelle et Politique de Madagascar (eds A. Grandidier &                         Wildlife: Threats and U.S. Policy. CRS report for Congress,
                G. Grandidier), vol. , pp. –. Imprimerie nationale, Paris,                            Damascus, USA.
                France.                                                                                 Y O U N G , R.P., V O L A H Y , A.T., B O U R O U , R., L E W I S , R., D U R B I N , J. & F A ,
             V E R Í S S I M O , D., C H A L L E N D E R , D.W.S. & N I J M A N , V. () Wildlife       J.E. () Estimating the population of the Endangered
                trade in Asia: start with the consumer. Asian Journal of                                   flat-tailed tortoise Pyxis planicauda in the deciduous, dry
                Conservation Biology, , –.                                                            forest of western Madagascar: a monitoring baseline. Oryx, ,
             W A L K E R , R.C. & R A F E L I A R I S O A , T.H. () Status of the relict               –.
                population of the Critically Endangered Madagascar spider tortoise                      Z H O U , Z. & J I A N G , Z. () International trade status and crisis for
                Pyxis arachnoides. Oryx, , –.                                                      snake species in China. Conservation Biology, , –.
             W A L K E R , R.C.J. () The internet based trade in Madagascar’s                       Z Y L S T R A , E.R., S T E I D L , R.J. & S WA N N , D.E. () Evaluating survey
                critically endangered tortoise species: A preliminary study                                methods for monitoring a rare vertebrate, the sonoran desert
                identifying the conservation threats. Testudo, , –.                                    tortoise. Journal of Wildlife Management, , –.

                                                                                             Oryx, 2020, 54(2), 188–196 © 2018 Fauna & Flora International doi:10.1017/S0030605317001880
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 10 Oct 2021 at 14:01:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001880
You can also read