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Ownership of parrots in Madagascar: extent and conservation implications - Cambridge University ...
Ownership of parrots in Madagascar: extent and
             conservation implications
                                                                                                          KIM E. REUTER, LUCIA RODRIGUEZ
                                                                         SAHONDRA               H A N I T R I N I A I N A and M E L I S S A S . S C H A E F E R

             Abstract The trade of live parrots is a threat to wild popula-                         they are extracted from source countries for international
             tions but is understudied. Madagascar is home to three par-                            pet markets (Poole & Shepherd, ). In Ghana, –%
             rot species listed on CITES Appendix II: Coracopsis nigra,                             of grey parrots Psittacus erithacus have been lost since
             Coracopsis vasa and Agapornis canus. Prior to this study                                as a result of the trade in these species and habitat deg-
             there were no data on the ownership of parrots in                                      radation (Annorbah et al., ). Likewise, in the
             Madagascar. We therefore aimed to investigate the extent                               Democratic Republic of Congo the live capture of parrots
             of the domestic pet trade in this group. Our objectives                                for the pet trade is a driver of the decline in P. erithacus
             were to quantify the prevalence, spatial extent, and timing                            (Hart et al., ). Although numerous studies have exam-
             of ownership. We collected data in July and August  in                             ined the keeping of parrots as pets in Latin America, there
             nine urban towns across Madagascar, using semi-structured                              have been relatively few studies of this in Africa.
             household surveys (n = ). We found that the ownership                                   Madagascar is home to three species of parrot: the lesser
             of pet parrots is widespread in time and space; % (% CI                            vasa parrot Coracopsis nigra, the greater vasa parrot
             –%) of interviewees had seen, and % (% CI –%)                                Coracopsis vasa and the grey-headed lovebird Agapornis
             had owned, a Coracopsis sp. Fewer interviewees (.% of all                            canus. There are no published population estimates for the
             interviewees) had seen A. canus in captivity, and only one in-                         three species, but all are thought to have at least , mature
             dividual reported having previously owned an A. canus. We                              individuals in the wild (BirdLife International, a,b,c). The
             estimate that , Coracopsis spp. individuals were held in                           live capture of parrots as pets in Madagascar has received
             captivity in the towns surveyed, in the . years prior to our                         scant attention (Martin et al., ), although other species
             interviews. It is likely that much of this ownership is illegal,                       are known to be threatened by live capture (Andreone et al.,
             although we did not examine this explicitly. Additional re-                            ; Schwitzer et al., ; Reuter et al., ).
             search is needed to determine whether current extraction                                   Most documented captures of live parrots in Madagascar
             rates are sustainable. This study adds to a growing body of evi-                       are anecdotal (McBride, ), outdated, or related to the
             dence that the domestic regulation of the trade of wild species                        legal export of live birds (UNEP-WCMC, ). In the
             is not being addressed adequately in Madagascar.                                       past there were reports from north-east Madagascar of wild-
                                                                                                    caught Coracopsis spp. being held prior to export for the
             Keywords Africa, Agapornis canus, birds, Coracopsis nigra,
                                                                                                    international pet trade (McBride, ), as well as in
             Coracopsis vasa, Madagascar, parrots, trade
                                                                                                    Antananarivo and around Tôlanaro for the domestic pet
                                                                                                    trade (C. vasa, Ekstrom, ; Coracopsis spp., Bollen &
                                                                                                    Donati, ). Evidence suggests that pet parrots within
                                                                                                    Madagascar are usually taken from the wild (as opposed
             Introduction
                                                                                                    to being bred in captivity; K. Reuter et al., unpubl. data;
                                                                                                    UNEP-WCMC, ).
             O     verexploitation is a threat to biodiversity (Baillie et al.,
                   ), with up to  million birds extracted alive
             from the wild annually (Karesh et al., ). Parrots
                                                                                                        Similar to other developing countries (Jepson & Ladle,
                                                                                                    ), there is little information regarding the trade and
             (Psittaciformes) are no exception; the trade in live parrots                           keeping of parrots as pets within Madagascar’s national
             is a threat to wild populations in many countries where                                boundaries. There are no data on the frequency of pet parrot
             they are endemic (Pires, ). Parrot populations across                              ownership within Madagascar, and estimates of extraction
             Africa are declining (Martin et al., ); in many cases                              are typically based on export data in the CITES database
                                                                                                    (Table ). However, in the absence of significant internation-
                                                                                                    al export (see Methods), there is a need for estimates of do-
             KIM E. REUTER (Corresponding author) Conservation International, Africa Field          mestic extraction. Understanding the domestic pet trade is
             Division, Nairobi, Kenya. E-mail kimeleanorreuter@gmail.com
                                                                                                    important for conservation programming. We aimed to in-
             LUCIA RODRIGUEZ and SAHONDRA HANITRINIAINA Pet Lemur Survey Initiative,
             housed by the University of Utah, Salt Lake City, Utah, USA
                                                                                                    vestigate the ownership of pet parrots (C. nigra, C. vasa,
                                                                                                    A. canus) in Madagascar. Our objectives were to quantify
             MELISSA S. SCHAEFER University of Utah, Salt Lake City, Utah, USA, and Salt Lake
             City Community College, Salt Lake City, Utah, USA                                      the prevalence, spatial extent and timing of ownership.
             Received  February . Revision requested  March .                            Based on identified gaps in the literature, we aimed to quan-
             Accepted  May . First published online  October .                           tify () the proportion of households that owned a parrot or

                                                                                        Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
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Ownership of parrots in Madagascar: extent and conservation implications - Cambridge University ...
Ownership of parrots in Madagascar                     583

           TABLE 1 Number of individuals of Coracopsis nigra, C. vasa and                         both Madagascar and the Comoros; BirdLife International,
           Agapornis canus exported from Madagascar since , including                         c).
           the number of parrots that were recorded as being wild caught                             Coracopsis nigra (Least Concern; stable population size;
           (UNEP-WCMC, ).
                                                                                                  BirdLife International, b) is a frugivore/granivore that
                                     No. of exported               Total no. of                   feeds in primary and secondary forests on ripe and unripe
                                     individuals recorded          individuals exported           fruit (Bollen & Elsacker, ; Reuter, ). In one study
           Species                   as wild caught                from Madagascar                the species was not found in edge or matrix habitats
           Coracopsis nigra          2,606                         5,875                          (Watson et al., ); other reports have found it in agricul-
           Coracopsis vasa           570                           4,242                          tural settings, forests, grasslands and savannahs (BirdLife
           Agapornis canus           54,469                        117,549                        International, b). The range of C. nigra is recorded as
                                                                                                  the entire island of Madagascar (, km; BirdLife
                                                                                                  International, b).
           had knowledge of parrot ownership, and () the occurrence                                 Agapornis canus (Least Concern; stable population size;
           of ownership in living memory. We estimated the number                                 BirdLife International, a) is a frugivore/granivore
           of Coracopsis spp. individuals extracted for pet ownership                             (Collar, ) found in coastal regions, with a large range
           in urban areas of Madagascar.                                                          that includes much of Madagascar (, km; BirdLife
                                                                                                  International, a). In one study the species was not
                                                                                                  found in edge or matrix habitats (Watson et al., ), al-
           Study area                                                                             though other sources indicate it is found in agricultural
                                                                                                  landscapes, savannahs and shrublands but not typically in
           The nine towns selected for surveying included five of the                             forests (BirdLife International, a).
           seven largest towns in Madagascar and the three in which                                  All three study species are listed in Appendix II of CITES
           published anecdotes indicated that Coracopsis spp. were                                ().
           kept as pets in the past (McBride, ; Ekstrom, ;
           Bollen & Donati, ). The towns are located in four of
           the country’s six provinces, and across all towns at least
           six ethnicities are represented. The combined human popu-                              Legality of capture, keeping and trade of wild parrots
           lation of the nine towns surveyed was c. . million, out of                          Within Madagascar a  law determined that species
           Madagascar’s total urban population of . million                                    listed in Appendix II of CITES () can be extracted (cap-
           (UNDP, ). Madagascar’s total population is c. .                                tured or hunted) legally only with a permit and within na-
           million people (World Bank, ). We acknowledge that                                 tional quotas determined by the government (Durbin,
           the survey effort could have both excluded and over-                                   ). Some have interpreted the law to mean that extrac-
           represented hotspots for parrot ownership. By selecting                                tion is further restricted to national hunting seasons
           areas where parrot ownership had been reported previously                              (Randrianandrianina et al., ). Similar to bushmeat
           in the literature, the sample could have been biased towards                           hunting (Golden et al., ; Reuter, ), it is likely that
           areas with higher ownership rates. However, there are areas                            most extraction occurs without permits and is therefore il-
           now known to the authors (e.g. Antsiranana) where parrots                              legal. Prior to , C. nigra was listed as a pest species and
           have been seen as pets but not reported in the literature, and                         could be hunted legally in the event of human–wildlife con-
           therefore this study could also have excluded areas where                              flict (Ekstrom, ).
           parrot ownership is popular but not previously known.                                      Export of these species from Madagascar is regulated
           Limited time and resources precluded surveying of more                                 (CITES, ). A moratorium on trade of C. vasa was issued
           areas.                                                                                 in  (Dowsett, ) after the government was unable to
                                                                                                  establish export quotas (although the primary threat to the
           Methods                                                                                species appeared to be habitat degradation; CITES, ). It
                                                                                                  was later recommended that this trade moratorium be lifted,
           Study species                                                                          given the low demand for the species from the pet trade
                                                                                                  (CITES, ). There have been no reported exports of
           Coracopsis vasa (categorized as Least Concern on the IUCN                              the species from Madagascar since  (UNEP-WCMC,
           Red List, but with a decreasing population; BirdLife                                   ). Regarding C. nigra, there have been no exports of
           International, c) is a frugivore/granivore that feeds in                           the species since , prior to which wild-caught individuals
           primary and secondary forests (Bollen & Elsacker, ;                                were exported for commercial reasons (UNEP-WCMC, ).
           Reuter, ). The species is edge-sensitive (Watson et al.,                           Agapornis canus captured from the wild continue to be ex-
           ). It is found in coastal regions, with a large range                              ported for commercial reasons ( individuals in  and
           that includes much of Madagascar (, km across                                    in ; UNEP-WCMC, ); an annual export quota

           Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
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https://doi.org/10.1017/S003060531700093X
584         K.E. Reuter et al.

             of , individuals was established in  (CITES
             Notification No. ) but was exceeded in the  years that
             followed (Species Survival Network, ). There is little
             evidence of substantial illegal export of the three species; a
             public database on illegal animal seizures did not list
             Madagascar’s parrot species (Wildlife Trade Tracker, ).

             Data collection

             We collected data in July and August  in  house-
             holds in nine towns across central, southern and eastern
             Madagascar, using semi-structured household surveys
             (Fig. ; Table ). Towns were selected at regular intervals
             along a  km highway transect (following Reuter et al.,
             ), beginning in Toamasina (eastern Madagascar) and
             travelling in a south-central direction via the RN/RN
             roads down to the town of Fianarantsoa. The town of
             Tôlanaro was not sampled using our overland transect ap-
             proach because of safety concerns regarding travel by car.                             FIG. 1 The provinces of Madagascar and the nine towns where
                 Based on Madagascar’s urban population and mean                                    interviews were conducted to investigate parrot ownership.
             household size (. people per household; INSTAT &
             ORC Macro, ), there are c. ,, urban households                              about whether they had owned a parrot, because of the po-
             in the country. It was therefore calculated that a minimum                             tential for increased interviewee discomfort. Some intervie-
             of  household interviews would yield a nationally repre-                            wees indicated voluntarily that they were current or former
             sentative dataset of urban Malagasy households (following                              owners. Therefore, rates of current and historical parrot
             Dillman, ; P set to %; margin of error ± % of the es-                           ownership could be ascertained only from information pro-
             timate; % confidence level).                                                         vided voluntarily by interviewees and should be considered
                 Verbal informed consent was received. Interviews were                              a conservative estimate.
             conducted by a two-person team of one international pro-                                  We did not provide interviewees with a definition of a pet
             ject leader (KER, LR, MSS) and one trained Malagasy trans-                             parrot, and individuals reported on both caged and uncaged
             lator (SH, see Acknowledgements). Following Reuter et al.                              birds. We anticipated a priori, given the physical similarities
             (), we used random sampling stratified by administra-                              between the two Coracopsis spp., that it would be difficult
             tive unit, with – interviews conducted within each of as                            for urban respondents to differentiate between C. nigra
             many communes/quarters within each town as time would                                  and C. vasa, especially if they saw the pet parrot only briefly.
             allow. To ensure independent sampling, only one adult was                              Therefore, aside from differentiating between Coracopsis
             interviewed per household. If an eligible individual refused                           spp. and A. canus (based on the respondent’s use of local
             to participate or if nobody was present, sampling continued                            or scientific names) no further species identification was
             at the next household. Interviews were anonymous and no                                done. We did not provide images of birds to facilitate species
             identifying information was collected.                                                 identification. When an interviewee did not recognize the
                 Interviewees were asked the following questions: () Have                          common names used by researchers, we occasionally
             you ever seen a pet parrot? () If so, where, when and how                             showed photographs of the three species on mobile phones.
             many did you see? We used various local words for parrots
             and lovebirds separately, as grey-headed lovebirds were not                            Analysis
             typically considered to be parrots by respondents.
             Translators were fluent in the local dialect and ensured                               Following similar studies (Reuter et al., ), and as there
             that the most appropriate common names were used. We                                   may be greater variation between than within towns, inter-
             excluded wild parrots or those seen in zoos, as this study                             viewees were used as subsamples within each town except
             was focused only on the ownership of parrots as pets.                                  for subsets of the data with low sample size. In other
             Noting that most pet parrots in Madagascar were probably                               words, towns were used as replicates in analyses unless
             extracted illegally (even if people were not aware that it was                         otherwise noted. Results are presented as mean values
             illegal; Keane et al., ), and following other survey efforts                       with % confidence intervals.
             in Madagascar regarding both legal and illegal behaviour                                  We estimated the total number of Coracopsis spp. held in
             (e.g. Reuter, ), we did not ask individuals directly                               urban households during  to mid  by extrapolating

                                                                                        Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
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https://doi.org/10.1017/S003060531700093X
Ownership of parrots in Madagascar                     585

           TABLE 2 Towns in Madagascar where interviews were conducted (Fig. ), with population, number of households interviewed, percentage of
           individuals who knew someone who owned or had previously owned a parrot, and percentage of individuals who themselves owned or had
           previously owned a parrot. Population estimates for cities were obtained from the Ilo Project ().

                                                                        No. of households              % interviewees who                 % interviewees who were current
           Town                                   Population            interviewed (%)                had seen a pet parrot*             or former parrot owners
           Ambositra                              32,818                62 (0.83)                      48                                 21
           Andasibe                               12,000                53 (1.94)                      11                                 17
           Antananarivo                           1,054,649             53 (0.02)                      23                                 11
           Antsirabe                              186,253               25 (0.06)                      68                                 0
           Beforona                               13,000                55 (1.86)                      38                                 6
           Fianarantsoa                           126,000               32 (0.11)                      25                                 3
           Moramanga                              40,050                60 (0.66)                      55                                 7
           Toamasina (Tamatave)                   201,729               50 (0.11)                      36                                 0
           Tôlanaro (Fort Dauphin)                46,298                50 (0.48)                      32                                 6
           Total                                  1,712,797             440 (0.11)                     37 (95% CI 26–48)                  8 (95% CI 3–15)
           *Does not include the respondents who had personally owned a parrot.

           the frequency of bird ownership at our urban sites to the                              , (% CI ,–,) Coracopsis spp. individuals
           towns in which data were collected, and also to all urban                              being held in captivity across the country in the . years
           areas in Madagascar. Following Reuter et al. (), we                                prior to our interview. Fewer interviewees (n = , or .%
           assumed conservatively that only one bird was owned per                                of all interviewees) had seen an A. canus in captivity. Only
           individual, representing one household.                                                one individual interviewed reported having previously
                                                                                                  owned an A. canus.

           Results                                                                                Timing of ownership Most people (% of  individuals)
                                                                                                  and most owners (% of  owners) could recall the year
           Profile of interviewees Most (%) interviewees were female,                           in which they saw or owned a pet Coracopsis sp. Most people
           % were male, and data were not collected in the remaining                            (% of  individuals) could recall the year in which they
           % of interviews (gender recorded in  interviews). All                              saw a pet A. canus, as could the one owner of this species
           were adults over the age of .                                                        interviewed. Many of these encounters occurred in the pre-
           Geographical extent of ownership Pet parrots had been seen                             vious  years (Table ). At least one respondent reported
           by respondents in all administrative regions where inter-                              having seen pet Coracopsis spp. in every decade since the
           views were conducted. They had also been seen elsewhere                                s and pet A. canus in every decade since the s.
           in the country (Fig. ).                                                               Respondents reported owning Coracopsis spp. in every dec-
                                                                                                  ade since the s, and the one owner of A. canus reported
           Proportion of respondents who had seen or owned parrots                                owning the pet in .
           Many interviewees (% (% CI –%); n =  over
           nine towns) had seen pet Coracopsis spp. (Table ). The pro-
           portion of interviewees who had seen a pet Coracopsis sp.                              Discussion
           varied by town (Pearson χ test: χ = ., N = , df = ,
           P , .). In addition, % (% CI –%) of interviewees                            Extent and patterns of ownership
           per town (range –%) had personally owned a pet
           Coracopsis sp. previously. Sample sizes (n =  owners                                 Based on our study and extrapolation to other urban areas of
           across nine towns) were too small to test whether the pro-                             Madagascar we estimate that , Coracopsis spp. indivi-
           portion of interviewees who had owned a pet Coracopsis sp.                             duals were held in captivity in the towns surveyed, in the
           varied by town. In the nine towns surveyed, .% (% CI                               . years prior to our interviews. For context, ,
           .–.%) of individuals interviewed had owned a pet                                   Coracopsis spp. individuals were exported from
           Coracopsis sp. in the . years prior to the interview (in                             Madagascar during – (UNEP-WCMC, ). As
            and ). An extrapolation suggests that an estimated                            mentioned in published reports, the domestic pet trade
           , Coracopsis spp. individuals were held in captivity in                            could be less of a threat nationally than habitat degradation
           the towns surveyed, in the . years prior to our interview                            (CITES, ) and hunting (Dowsett, ; Ekstrom,
           (using town-specific rates of ownership for extrapolation).                            ); more research on this topic is required. Ownership
           Extrapolating the .% (% CI .–.%) estimate to all                               of A. canus was relatively low; so low that we could not ex-
           urban households in Madagascar yields an estimate of                                   trapolate to the rest of Madagascar. Overall, the frequency of

           Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
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https://doi.org/10.1017/S003060531700093X
586         K.E. Reuter et al.

                                                                                                                                          FIG. 2 Locations in Madagascar
                                                                                                                                          where interviewees reported seeing
                                                                                                                                          (a) Coracopsis spp. and (b)
                                                                                                                                          Agapornis canus individuals kept
                                                                                                                                          as pets.

             pet parrot ownership in Madagascar (% (% CI –%) of                               interviewees in some towns (Table ). In one case, a pet par-
             households) may be low compared to other countries (%                                rot was owned collectively by the staff of a police station.
             of Costa Rican households have kept parrots as pets, Drews,
             ; .% of Indonesian households surveyed had pet
             birds, Jepson & Ladle, ), although it appears to be                                Conservation implications
             high in some towns.
                The ownership of pet parrots appears to be widespread in                            We cannot ascertain whether the in-country ownership of
             time and space, but more extensive surveys are required to                             pet parrots is sustainable, because there is a lack of published
             investigate the hotspots of ownership. We found evidence of                            information about these species (e.g. population estimates)
             in-country ownership of Coracopsis spp. and A. canus going                             and their ownership as pets (e.g. longevity in captivity, age
             back several decades. In similar, recent research on the in-                           of capture). As such, we cannot estimate extraction rates for
             country ownership of lemurs, respondents could recall see-                             these species. Information on longevity in captivity and age
             ing captive lemurs in Madagascar in the s (Reuter et al.,                          of capture would be a useful avenue for future studies. In a
             ).                                                                                 well-kept captive environment, the maximum lifespan
                Although not indicated directly by our dataset, our find-                           in captivity has been reported as ,  and  years for
             ings indicate that compared to the ownership of pet lemurs,                            C. nigra, C. vasa and A. canus, respectively (Young et al.,
             the ownership of pet parrots is relatively visible in urban                            ). Therefore, the parrots could conceivably be moved
             areas of Madagascar. This is the case even though most of                              among and between multiple owners over time. However,
             the observed parrot ownership would probably be consid-                                in Madagascar, Coracopsis spp. may be kept in captivity
             ered illegal. Perhaps this reflects a low awareness regarding                          for much shorter periods of time (K. Reuter et al., unpubl.
             environmental laws in Madagascar (Keane et al., ), poor                            data), perhaps because (as we observed anecdotally) pet par-
             enforcement of laws, and/or that ownership is not asso-                                rots are kept in environments that do not facilitate adequate
             ciated with social stigma. Over one-third of respondents re-                           movement and nutrition. Regarding the age of capture, un-
             ported having seen a Coracopsis sp. as a pet, and we saw                               like studies from elsewhere (e.g. Jepson, ), we do not
             parrots kept in cages on balconies of households that were                             know whether there is a tendency to catch wild parrots
             not selected for interviews. Unlike when conducting surveys                            at certain life stages (e.g. young, crop-raiding birds or breed-
             related to the illegal ownership of lemurs (Reuter et al.,                             ing adults), although both adults and juveniles of C. vasa
             ), we did not sense a fear of enforcement or repercus-                             and A. canus are reportedly captured as pets (BirdLife
             sions as a consequence of participation in the survey.                                 International, a,b). Should the extraction of parrots
             Respondents did not hesitate to show researchers their pet                             for the pet trade be unsustainable, the resulting decrease
             parrots, and self-reported ownership rates were up to % of                           in parrot populations could have negative implications for

                                                                                        Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
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https://doi.org/10.1017/S003060531700093X
Ownership of parrots in Madagascar                     587

           ecosystem health. In several remnant forests in Madagascar,                            Author contributions
           C. vasa and C. nigra are among only a few frugivorous bird
           species (Bollen & Elsacker, ; Reuter, ). As such, they                         KER and MSS designed the project, and KER secured funding.
           are considered to be important seed dispersers (Reuter,                                All authors collected, analysed and interpreted data, wrote and
           ). In other areas of the developing world, market-based                            undertook a critical revision of the article, and approved the
           solutions (such as commercial breeding of popular bird spe-                            final article for publication.
           cies) have been proposed to shift bird-keeping from wild-
           caught to captive-bred individuals (Jepson & Ladle, ;
           Jepson et al., ). These market-based and voluntary me-                             References
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                                                                                                        Oryx, 2019, 53(3), 582–588 © 2017 Fauna & Flora International doi:10.1017/S003060531700093X
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 29 Jan 2021 at 12:47:32, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
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