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Emu - Austral Ornithology
ISSN: 0158-4197 (Print) 1448-5540 (Online) Journal homepage: http://www.tandfonline.com/loi/temu20
Grey areas: temporal and geographical dynamics
of international trade of Grey and Timneh Parrots
(Psittacus erithacus and P. timneh) under CITES
R. O. Martin
To cite this article: R. O. Martin (2017): Grey areas: temporal and geographical dynamics of
international trade of Grey and Timneh Parrots (Psittacus erithacus and P. timneh) under CITES,
Emu - Austral Ornithology
To link to this article: http://dx.doi.org/10.1080/01584197.2017.1369854
Published online: 14 Sep 2017.
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Grey areas: temporal and geographical dynamics of international trade of Grey
and Timneh Parrots (Psittacus erithacus and P. timneh) under CITES
R. O. Martin
a,b
a
Africa Programme, World Parrot Trust, Hayle, UK;
b
FitzPatrick Institute of African Ornithology DST-NRF Centre of Excellence, Department of
Biological Sciences, University of Cape Town, Cape Town, South Africa
ABSTRACT
International trade in wild birds is a driver of biodiversity loss, species invasions and the spread of
diseases. Grey and Timneh Parrots (Psittacus erithacus and P. timneh) have been among the most
frequently traded of all birds listed in the Appendices of the Convention on International Trade in
Endangered Species of Wild Fauna and Flora (CITES) and were recently categorised as Endangered
on the IUCN Red List. Records of international trade, available on the CITES trade database, were
used to establish geographical trends in imports and exports of Grey and Timneh Parrots since
1975. Patterns of trade varied dramatically over time, with key trading partnerships changing
frequently. Net exports of over 1.2 million wild-sourced parrots were reported, the majority of
which were exported to North America prior to 1992 and Europe prior to 2005. Recently, there
has been a rapid rise in exports of captive-bred parrots to parts of Asia, notably countries in the
Arabian Peninsula. The majority of captive-bred Grey and Timneh Parrots originate from South
Africa, which has at times also been the largest importer of wild-sourced parrots. Patterns of trade
are considered in the context of the changing economic, cultural, governance, and biological
circumstances to understand the potential drivers of major shifts and identify research needs and
interventions to control trade.
ARTICLE HISTORY
Received 2 May 2017
Accepted 11 August 2017
KEYWORDS
Wild bird trade; trade
regulation; CITES; species
conservation; exotic pet
trade; captive breeding;
parrots
Introduction
Parrots (order Psittaciformes) have long been
trapped in large numbers in the wild for the inter-
national pet bird trade (Beissinger 2001). Since the
inception of the Convention on International Trade
in Endangered Species of Wild Fauna and Flora
(CITES), approximately 12 million live parrots have
been reported in international trade, the majority of
which (62%) were either wild-sourced or of
unknown origin (UNODC 2016). The potential
threats to wild populations posed by this trade have
led to the entire order being listed in the Appendices
of CITES, with the exception of four relatively com-
monspecies.Inadditiontotheoverexploitationof
wild populations (Wright et al.2001;González2003;
Pain et al.2006; Clarke and Rolf 2013), the wild bird
trade has been linked to a number of issues of con-
servation, economic and human health concern,
including the establishment of alien species (Cassey
et al.2004,2015; Carrete and Tella 2008; Cardador
et al.2017) and the spread of infectious diseases
(Karesh et al.2007; Varsani et al.2011; Harkins
et al.2014). The development of effective policies
and interventions to mitigate the threats posed by
the global bird trade requires an understanding of
current and historical trade patterns and their
drivers.
Several African parrot species have regularly ranked
among the most traded of all bird species listed under
CITES. Between 2010 and 2014, three of the top four
most traded birds listed in the CITES Appendices were
endemic to Africa (Psittacus erithacus,Poicephalus
senegalus and Poicephalus gulielmi)(www.dashboards.
cites.org: UNEP WCMC, Cambridge, UK, downloaded
14 April 2017). High levels of exploitation have been
identified as a threat to wild populations for several of
the larger parrot species in Africa (Perrin 2012; Martin
et al.2014). A recent analysis concluded that the most
common threat to parrots in the Afro-tropics was
hunting and trapping, primarily for the cage-bird
trade and for use as pets (Olah et al.2016).
Grey and Timneh Parrots (Psittacus erithacus and P.
timneh) are native to the moist forests of the Afro-
tropics, their distribution spanning 21 countries in
West, Central and East Africa (Forshaw and Cooper
1989). Until recently these taxa were considered
together to comprise a single species, Psittacus
CONTACT R. O. Martin rmartin@parrots.org
EMU - AUSTRAL ORNITHOLOGY, 2017
https://doi.org/10.1080/01584197.2017.1369854
© 2017 BirdLife Australia
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erithacus. Following taxonomic reassessment (Del
Hoyo and Collar 2014) this one species was split by
some authorities into two species, the Timneh Parrot
(P. timneh), restricted to West Africa from Guinea-
Bissau to Côte d’Ivoire, and the Grey Parrot (P. eritha-
cus), occurring from eastern Côte d’Ivoire through the
forests of the Congo Basin to Kenya and Tanzania.
This split has not yet been recognised by CITES, and
in keeping with this nomenclature hereafter both taxa
are referred to collectively as Psittacus parrots.
Although Psittacus parrots can be bred in commercial
quantities in captivity, the relative ease with which
large numbers can be captured from the wild and
transported to markets means that wild-sourced birds
have remained a common source of pet birds as well as
breeding stock for aviculturists. Recent data have rein-
forced earlier anecdotal reports that populations of
Psittacus parrots have suffered rapid declines in parts
of their range as a result of trade and forest loss
(Annorbah et al.2016). In Ghana, which exported
large numbers of Psittacus parrots in the past, systema-
tic field surveys indicate that populations have col-
lapsed by as much as 90–99% since the early 1990s, a
time when fieldworkers were already voicing concerns
about declining populations (Grimes 1983; Dändliker
1992a). Additional surveys have recorded very low
population densities in parts of West Africa (Marsden
et al.2016) and Central Africa (Maisels and Stringberg
2016). Parrot traders recently arriving in previously
unexploited forest areas of the Congo Basin report
declining harvests in historical trapping sites, suggest-
ing that overexploitation of wild populations may be
widespread (Hart et al.2016). In 2016 Grey and
Timneh Parrots were uplisted to Endangered on the
IUCN Red List of Threatened Species on the basis that
‘the extent of the annual harvest for international trade,
in combination with the rate of ongoing habitat loss,
means it is now suspected to be undergoing rapid
declines over three generations (47 years)’(BirdLife
International 2017).
CITES is the principal multilateral treaty through
which global trade in wildlife is regulated. Since its
inception in 1975, 183 states have become Parties to
the convention, thereby agreeing to ensure that inter-
national trade in specimens of wild animals and plants
does not threaten their survival. CITES requires that all
exports of species listed in Appendices I and II are
accompanied by an export permit, and Parties must
submit annual reports on exports and imports to the
CITES Secretariat. In 1981, Psittacus parrots were
transferred from Appendix III to Appendix II on the
basis that regulation of trade is necessary to avoid
utilisation incompatible with the survival of the species
in the wild. Under Appendix II, Parties have been
encouraged to establish science-based export quotas,
and processes, such as the Review of Significant
Trade, have produced recommendations for improving
management of the trade such as conservative export
quotas and moratoria on exports. In light of declines in
wild populations and ongoing compliance issues,
CITES Parties voted at the Seventeenth Conference of
Parties (Johannesburg, South Africa, 24 September to 5
October 2016) to adopt a proposal submitted by five
range states and four other CITES Parties to transfer
Psittacus parrots to Appendix I (Proposal no. 19;
CITES 2016). As a result of this decision, from
January 2017 international trade in wild-sourced
Psittacus parrots for commercial purposes is no longer
permitted. However, three Parties, including one major
exporting country (the Democratic Republic of Congo)
and two importing countries (the UAE and Saudi
Arabia), entered reservations to the listing, meaning
that trade between these countries could continue as
if the species were still listed in Appendix II.
In this study, records of imports and exports of
Psittacus parrots submitted to CITES are used to inves-
tigate the patterns of trade in Psittacus parrots since
1975. Focus is placed on geographical trends in imports
and exports of wild-sourced and captive-bred Psittacus
parrots to identify how key trading partnerships have
changed over time. The scale of recent compliance
issues, as indicated by CITES trade data, is also quan-
tified. Although several peer-reviewed studies and
reports have previously interrogated CITES data on
Psittacus parrots (CITES 2006; Li and Jiang 2014;
UNODC 2016;Poole and Shepherd 2017), no pub-
lished assessments of global trade patterns currently
exist. Through characterising the trade and exploring
patterns in the context of historical events and inter-
ventions to improve regulation, I aim in this paper to
address this shortfall and provide a quantitative basis
for decision making around the management of inter-
national trade in Psittacus parrots.
Methods
Data on the legal trade in live Psittacus parrots for
commercial purposes were downloaded directly from
the CITES database (www.trade.cites.org: UNEP
WCMC, Cambridge UK, downloaded 14 April 2016).
This database holds records of the import, export and
re-export of CITES-listed species as reported to the
CITES Secretariat by Parties to CITES. Reporting of
these data is mandatory under the Convention, high-
lighted in CITES Article VII, which requires each Party
to maintain trade records for all CITES-listed species
2R. O. MARTIN
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(CITES 1979). Three different outputs were down-
loaded from the database for the period between 1975
and 2014: (1) a comparative tabulation report, which
details quantities traded annually between trading part-
ners as reported by both importers and exporters, (2) a
net (re-)export report, which details the net balance of
quantities exported minus quantities imported, (3) and
net imports, which similarly details the net balance of
imports minus exports. In situations where quantities
reported by importers and exporters vary, the higher
figure was taken to represent the quantity in trade.
Differences in reported levels of trade can occur for a
variety of reasons including clerical errors, one party
failing to report on transactions, specimens being
exported at the end of one year but not received by
the importer until the following year and differences in
the way that Parties record and report transactions
(Phelps et al.2010; CITES 2013a). Under the
Convention, records must as far as possible report the
actual trade that took place (i.e. the quantity of speci-
mens that entered or left the country) but under Article
VIII Parties are also permitted to report trade based on
the permits issued. These variables mean that the
extent to which trade figures reflect actual levels is
uncertain, but nevertheless these data remain the
most comprehensive long-term database of interna-
tional transactions of wildlife in existence and have
proved valuable for identifying patterns of trade (e.g.
Heinrich et al.2016; Vall-llosera and Cassey 2017).
Although CITES does not recognise the split of
Psittacus parrots into two distinct species (P. erithacus
and P. timneh), some records within the CITES data-
base identify shipments as Timneh Parrots. However,
theextenttowhichthemajorityofrecordsreported
by Parties reflect the particular taxa involved is
unclear. In light of this, all records belonging to the
genus Psittacus were downloaded and no attempt has
been made in this study to distinguish trade in
Timneh and Grey Parrots.
To visualise the network of the trade in Psittacus
parrots and how this has varied over time, network
diagrams to represent the flow of Psittacus parrots
between countries were constructed. In these diagrams
each node represents a country that has reported trade,
and arrows connecting nodes (links) indicate the direc-
tion, volume (number of reported specimens) and
source (captive-bred, wild-sourced or other) of trade.
Geographical regions to which each country belongs
are indicated by node colour and regional affinities of
countries were designated in accordance with the
United Nations geoscheme. Diagrams were constructed
within the R statistical environment (Version 3.2.2, R
Core Team 2015) using the package ‘igraph’(Csardi
and Nepusz 2006) and used a Fruchterman-Reingold
force-directed layout algorithm (Fruchterman and
Reingold 1991). This algorithm positions nodes in rela-
tion to each other, based on the volumes of trade
between them. Clusters of nodes therefore provide an
indication of groups of key trading partners. Focus was
on major partnerships, and only transactions involving
more than 800 specimens, aggregated over each illu-
strated time period, were included in visualisations.
Results
Overall levels of trade
Net exports of 1 644 037 Psittacus parrots were reported in
trade between 1975 and 2014. Of these, 1 224 755 (74%)
were reportedly wild-sourced, 403 410 (25%) captive-bred,
and a further 15 872 (1%) were of unknown source.
Commercial shipments of wild-sourced Psittacus
parrots (Purpose code ‘T’, Source code ‘W’) have
been reported from 77 countries and imports into
123. However, the majority of these shipments involved
relatively small quantities and over 90% of exports were
reportedly from just eight countries (seven range states
and Senegal). Shipments of wild-sourced birds have
been reported from the majority of range states with
the exception of Rwanda and Angola; however, Angola
only became a party to CITES in 2013.
Commercial exports of captive-bred Psittacus parrots
(Purpose code ‘T’,Sourcecode‘C’) have been reported
from 90 countries and into 139. Ninety per cent of
exports were accounted for by just eight countries,
including two range states with no known breeding facil-
ities. Captive-bred exports were dominated by South
Africa, which alone accounted for 67% of all exports.
Trends over time
The relative importance of wild vs. captive-sourced
Parrots as well as patterns of importing and exporting
countries changed dramatically during the study per-
iod, and based on these changes the international trade
can be broadly categorised into three distinct periods:
(i) 1975–1992, (ii) 1993–2005, and (iii) 2006–2014.
Between 1975 and 1992 wild-sourced Psittacus parrots
dominated international trade, accounting for 97% of all
reported trade. Annual exports varied considerably over
the period, increasing from fewer than 5000 Parrots per
year prior to 1980 to an all-time peak of more than 63 000
in 1988 and remaining above 50 000 until 1992 (Figure 1
(a)). Exports of the majority (71%) of these wild-sourced
Parrots originated from West Africa and this dominance
was particularly the case at the peak of exports in 1988
EMU - AUSTRAL ORNITHOLOGY 3
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(Figure 1(b)). A decline in exports from West Africa
towards the end of the period was to some extent offset
by a gradual rise in exports from Central Africa, with
exports from Central Africa approximately doubling
between the mid-1980s and 1992. During this period,
imports were largely to North America and Europe,
which respectively accounted for 47% and 43% of
imports. Southern Africa, principally South Africa, was
the third largest importing region accounting for 6% of
imports (Figures 1(c) and 2(a)).
Exports of wild-sourced parrots remained high
between 1993 and 2005, although generally lower
than exports in the late 1980s and early 1990s
(Figure 1(a)). Wild-sourced parrots continued to
Figure 1. Annual trade in live Psittacus parrots globally for the period 1975–2014summarisedby(a)netexports by source, (b) net exports
by region, and (c) net imports by region (dashed lines indicate captive-bred exports, solid lines indicate wild-sourced exports).
4R. O. MARTIN
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dominate exports throughout the period until a dra-
matic reduction in 2005, from which point onwards
captive-bred parrots became more frequently reported.
A rapid increase in exports of captive-bred parrots
occurred during this period, rising from a relatively
negligible volume to over 20 000 in 2005. The period
was dominated by a dramatic shift in the origins of
wild-sourced parrots away from West Africa towards
Central Africa. Over the period, exports from Central
Africa were consistently much higher than those from
West Africa and accounted for 82% of all wild-sourced
parrots between 1993 and 2005 (Figure 1(b)). During
this period, Europe became the predominant importer,
experiencing a modest increase in imports to account
for 73% of trade (Figure 1(c)). In contrast, imports to
North America all but ceased (Figure 2(a,b)), while
imports to Southern Africa remained largely stable.
Notably, there was a rise, particularly in the latter half
of the period of imports into Eastern and South-eastern
(notably captive-bred parrots to Thailand, Singapore,
Japan, Hong Kong and China and wild-sourced into
Singapore and Thailand, listed in diminishing order of
Figure 2. International trade networks of live Psittacus parrots during three phases of trade (a) 1975–1992, (b) 1993–2005, and (c)
2006–2014. Networks are based only on trade links which account for more than 800 specimens over each period. Nodes represent
individual countries, with node labels indicating the UN two-letter code for each country (country names given below). Node colour
indicates the geopolitical region to which each country belongs and node size indicates connectedness (size proportional to the natural
log of the number of direct trade links). Arrows indicate the direction of trade flows. Arrow width is proportional to the numbers of
specimens traded and arrow colour indicates the source (captive-bred, wild-sourced or other). Country codes: AE = United Arab Emirates,
AM = Armenia, AT = Austria, BD = Bangladesh, BE = Belgium, BH = Bahrain, CA = Canada, CD = Congo, the Democratic Republic of the,
CF = Central African Republic, CG = Congo, Republic of, CH = Switzerland, CI = Cote d’Ivoire, CM = Cameroon, CN = China, CZ = Czech
Republic, DE= Germany, ES = Spain, FR = France, GB = United Kingdom, GH= Ghana, GN = Guinea, GQ = Equatorial Guinea, GR = Greece,
HK = Hong Kong, ID = Indonesia, IL = Israel, IT = Italy, JO = Jordan, JP = Japan, KW = Kuwait, LB = Lebanon, LR = Liberia, LY = Libya,
ML = Mali, MT = Malta, MX = Mexico, MY = Malaysia, NL = Netherlands, NO = Norway, OM = Oman, PH = Philippines, PL = Poland,
PT = Portugal, QA = Qatar, RS = Serbia, RU = Russian Federation, SE = Sweden, SL = Sierra Leone, SG = Singapore, SN = Senegal,
TG = Togo, TH = Thailand, TR = Turkey, TW = Taiwan, US = United States, UZ = Uzbekistan, ZA = South Africa.
EMU - AUSTRAL ORNITHOLOGY 5
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importance) and Western Asia (notably captive-bred
parrots to the UAE, Israel and Kuwait and wild-
sourced to Israel, Kuwait and Qatar) (Figures 1(c)
and 2(b)).
The period 2006–2014 was characterised by a dra-
matic rise in net exports to over 100 000, the highest
number of Psittacus parrots reported in trade in any
single year in this study (Figure 1(a)). This steep rise
was driven largely by increases in the number of cap-
tive-bred birds, which surpassed wild-sourced exports
for the first time in 2007, and accounted for 73% of all
trade during the period (Figures 1(a) and 2(c)). Wild-
sourced exports saw a relatively modest rise from both
Central and West Africa, although Central Africa
(notably the DRC) continued to dominate exports
(Figures 1(b) and 2(c)). The largest proportion of
exports from Central Africa went to South Africa,
although notable numbers also moved to Singapore,
other Asian countries and also Serbia (Figure 2(c)).
The majority of captive-bred birds exported during
this period originated from South Africa and were
imported into Western Asia, notably the Arabian
Peninsula, which saw an explosion of imports over
the period (Figures 1(c) and 2(c)). These birds were
also moved in considerable numbers among countries
in the Arabian Peninsula, as demonstrated by the clus-
tering of these countries in Figure 2(c). Large numbers
of captive-bred birds were also imported into countries
in Central, Southern and South-eastern Asia, notably
Pakistan, Malaysia, Hong Kong and Singapore (Figures
1(c) and 2(c)).
Indicators of compliance with CITES: 2006–2014
Since 2006, reported net exports of wild-sourced birds
have exceeded published annual export quotas from at
least one country every year with the exception of 2007.
Reported exports during this period exceeded pub-
lished quotas by 42 965, the majority (92%) of which
were reported to have been exported from the DRC
(Table 1). Excesses were also reported for Guinea,
which had zero export quotas for much of this period
and Cameroon which exported 900 in excess of zero
export quotas between 2008 and 2011. In addition 2200
wild-sourced parrots originating from the DRC and the
Republic of Congo were re-exported from Guinea.
A further 16 963 were reportedly exported from
countries that had no published quota (Table 1). The
majority (70%) of these were exported between 2012
and 2014 from the Republic of Congo, which reported
exports in adherence to an export quota of 4000 per
year between 2007 and 2011. Cameroon accounted for
much of the remainder of the exports (28%), with
smaller numbers being exported from Benin and
Togo. In 2013 the Republic of Congo also re-exported
200 Timneh Parrots reportedly originating from
Guinea.
Net exports of 4679 were also reported from several
countries that have been considered range states but
are not known to have any, or host only negligible, wild
populations (Table 1). Notable among these were Mali,
which exported 2570 Grey Parrots and 1520 Timneh
Parrots. Smaller numbers were also exported from
Benin (74) and Togo (80). Wild-sourced parrots with
no declared country of origin were exported from
Mozambique (435) and South Africa (360).
Net exports of 13 264 were reported as ‘captive-bred’
exports from range states that have no known com-
mercial breeding facilities (Table 1). Of these, 52% were
exported from the Central African Republic, 28% from
Guinea (including both Grey and Timneh Parrots), and
10% from Côte d’Ivoire, with smaller numbers from
Cameroon, the DRC and Nigeria. If these exports were
in fact wild-sourced this suggests the true number of
wild-sourced parrots in reported trade is 12% higher
than official figures indicate. In addition to these num-
bers, Mali exported a further 1116 as captive-bred and
re-exports of 5037 from South Africa and Saudi Arabia.
Discussion
Trade reported to CITES suggests very large volumes
of Psittacus parrots have been trapped in the wild for
the exotic pet trade since 1975. Although limits to
CITES data make it difficult to determine accurate
levels of trade (Phelps et al.2010), compliance issues
such as the apparent misreporting of wild specimens as
Table 1. Net exports of wild-sourced and captive-bred
Psittacus parrots indicative of compliance with CITES between
2007 and 2014
Country
Exports in
excess of
published
annual
quota
Exports in
absence
of
published
annual
quota
Exports of wild-
sourced parrots
where no or
negligible wild
populations
occur
Exports of
captive-bred
parrots where
no commercial
breeding
facilities occur
Cote d’Ivoire –– – 1400
Guinea 2500 220 –4325
DRC 39 565 –– 150
Congo –12 035 ––
Cameroon 900 4708 –300
CAR –– – 7020
Nigeria –– – 300
Togo –– 80 –
Benin –– 64 –
Mali –– 4090 –
Mozambique –– 435 –
South Africa –– 360 –
Total 42 965 16 963 5029 13 495
6R. O. MARTIN
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captive-bred (CITES 2012a) suggest that official figures
may underestimate the number of wild-sourced parrots
in reported trade. In addition, high levels of pre-export
mortality (variously estimated at between 10 and 66%;
Fotso 1998a, 1998b; McGowan 2001; Clemmons 2003;
Hart 2013), unreported illegal trade and trade within
domestic markets suggest that the true numbers of
parrots trapped over this period may be considerably
greater than the 1.22 million reported here.
Drivers of change in trade in Psittacus parrots
reported to CITES
Marked regional shifts in the key exporting and
importing countries indicate a dynamic global trade
underpinned by several trading hubs. Shifting pat-
terns of imports, exports and re-exports are likely
driven by a number of regulatory changes including
CITES measures, unilateral restrictions on imports
and exports and social, economic and biological fac-
tors affecting supply and demand.
The first major shift occurred in the early 1990s,
when overall trade in wild birds showed a marked
decline, particularly from West Africa, and imports
into North America, one of the key markets in the
1980s, all but ceased. Starting in 1988, exports from
several range states were scrutinised as part of phase
one of the CITES Review of Significant Trade (RST)
initiated in 1988. As a result of the review process, two
field studies were conducted to evaluate the status of
wild populations and the impact of trade in West
Africa, focusing on Guinea and Ghana (Dändliker
1992a,1992b). Both of these studies highlighted con-
cerns that current levels of trade were unsustainable.
Indeed, annual exports from Guinea exceeded the
population estimate for the entire country at that
time, suggesting that many exported parrots may have
in fact originated from other countries (Dändliker
1992a). In Ghana, anecdotal reports reinforced the ear-
lier concerns of others (Grimes 1983) that populations
had been greatly reduced due to trapping (Dändliker
1992a). Concerns were also raised about large numbers
of exports from Togo, despite having almost no viable
population, as well as exports from Côte d’Ivoire
(Dändliker 1992a). Following the review, recommenda-
tions were made for Cameroon, Ghana, Guinea, Liberia
and Togo. Exports from several countries, including
Mali, Côte d’Ivoire, Ghana, Guinea and Togo largely
ceased at this time, although some of these countries
resumed exports in the 2000s at relatively low levels
(CITES 2012b).
At about the same time, imports of wild birds into
the United States ceased as a result of the passing of the
1992 Wild Bird Conservation Act (WBCA). Prior to the
passing of the Act, the United States was a major
importer of wild-sourced Psittacus parrots from West
as well as Central Africa (Figure 2(a)). European Union
bans on imports from several West African states,
including Ghana and Togo, also came into existence
in the late 1980s (Mulliken 1995). Although it appears
that alternative markets for Psittacus parrots from
West Africa were not readily available, a spike in
imports into South Africa at this time may reflect the
redirection of some legal exports from West Africa,
and potentially illegal exports (Mulliken 1995).
The reduction in exports from West African coun-
tries may also have been driven by a decline in the
availability of wild birds in the region. Recent surveys
in Ghana indicate that populations have declined by
90–99% since the early 1990s, and extensive searches
found none of the large roosts which once reportedly
hosted thousands of Grey Parrots (Annorbah et al.
2016). Recent surveys in other countries in West
Africa suggest densities are also low in other areas
(Marsden et al.2016), potentially precluding exports
on the massive scales (over 40 000 per year) that
occured for much of the 1980s. A field study in
Nigeria in 2001 found that 100% of known nests were
being poached, indicating that exploitation was occur-
ring at maximum and unsustainable levels (McGowan
2001; Pain et al.2006). A number of studies have
suggested that measures of availability, such as the
abundance and accessibility of wild populations, are
particularly important in determining levels of trade
in some groups of parrots (Pires and Clarke 2012;
Pires 2015; Vall-llosera and Cassey 2017; but see Tella
and Hiraldo 2014).
A second major shift in trade patterns occurred in
the mid-2000s, when trade in wild-sourced Psittacus
parrots declined and volumes of captive-bred parrots
continued to increase rapidly. The decline in trade in
wild-sourced birds coincided with a number of events
affecting the regulation of international trade. Among
these, the rapid global spread of the highly pathogenic
and zoonotic H5N1 strain of the avian influenza virus,
which emerged in 2003, led to the implementation of
numerous restrictions on trade in many importing
countries (e.g. Brooks-Moizer et al.2008). Among
them the European Union, which was by far the largest
importer of wild-sourced parrots from the mid-1990s
to mid-2000s, and a significant market for those bred
in captivity, placed a temporary suspension on imports
of all wild birds in 2005, which was made permanent in
2007 on the basis of recommendations of biosecurity
and animal welfare. In addition, in 2006 restrictions on
exports from the principal exporting range states were
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recommended as a result of the CITES RST process.
These included temporary suspensions on exports from
Cameroon, Côte d’Ivoire, Guinea, Liberia and Sierra
Leone, and conservative quotas for the DRC and the
Republic of Congo (CITES 2006). Several countries in
West Africa effectively ceased exports at this time,
publishing export quotas of zero from 2007 onwards
to which they largely adhered (CITES 2012a).
However, in Guinea, exports reported as captive-bred
increased dramatically despite there being no captive
breeding of CITES-listed species occurring in Guinea,
suggesting that the source was being mislabelled
(CITES 2012b).
The increase in exports reported as captive-bred is
largely accounted for by rising exports from South
Africa, which came to dominate global exports by the
mid-2010s. The initial rise in exports in the mid-1990s
may in part be attributable to the mislabelling of re-exports
of wild-sourced birds that were both legally and illegally
imported into South Africa, largely from West Africa
(Mulliken 1995). Also at this time, the ready availability
of wild-sourced parrots and the refinement of techniques
for the captive breeding of Psittacus parrots in South Africa
paved the way for the establishment of large-scale breeding
facilities for export, relying on relatively inexpensive wild-
sourced birds (Mulliken 1995). This industry was highly
lucrative and a financial evaluation conducted in 2004
suggested that the establishment of a relatively small breed-
ing facility (32 pairs) could generate annual returns of 62%
on capital investment (Dennison 2004). In recent years
there has been considerable investment in avicultural facil-
ities in South Africa, which has emerged as by far the
largest exporter of CITES-listed birds. By 2015 it was
estimated that South Africa had over 1600 breeding facil-
ities, of which 5–10 were ‘mega-facilities’with 500–1000
pairs (PASA pers. comm. 2015). Until 2012 South Africa
also continued to be one of the principal importers of wild-
sourced Psittacus parrots, the majority of which originated
from the DRC (Figure 2(c)). Wild parrots are preferred by
some breeders as they are relatively inexpensive and have
the potential to breed immediately, compared with a wait
of 4–5 years for those bred in captivity (Dennison 2004).
Since 2007, the majority of captive-bred parrots in
trade were imported into countries in the Arabian
Peninsula and to a lesser degree Central and South-east-
ern Asia (Figure 2(c)). Interestingly, substantial volumes
of parrots were re-exported between countries in the
Arabian Peninsula, suggesting the existence of a close-
knit trade network (Figure 2(c)). Of particular note is the
role of Bahrain, which was one of the largest importers
during this period, yet only became a signatory to CITES
in 2012. Although the majority of reported trade in the
region largely comprises captive-bred parrots originating
in South Africa, there were also substantial imports of
wild-sourced parrots from the DRC and the Republic of
Congo. The growth in imports of Psittacus parrots into
Asia may reflect a generally expanding consumer com-
munity for wildlife including exotic pets, which may be
attributable to a number of factors including rapid
human population growth, increasing affluence, expan-
sion in international travel routes, Internet connectivity
and cultural shifts (Ding et al.2008;McNeelyet al.2009;
Bush et al.2014).
The future of trade in Psittacus parrots:
challenges and opportunities
The dynamics of trade over the last 40 years highlights
some of the challenges and opportunities for regulating
international trade in parrots. Although the available
data preclude detailed analysis of the impact of regula-
tory measures vs. the economic, cultural and biological
factors that determine supply and demand in interna-
tional markets, it appears evident that specific regula-
tory changes brought about unilaterally and through
international conventions such as CITES have resulted
in changes in the flow of trade as reported to CITES.
While it has been suggested that the restriction of
imports into the United States and European Union
had little influence on overall levels of reported trade in
parrots globally (Cardador et al.2017), it appears that
the effective removal of large pools of potential con-
sumers had immediate and long-lasting impacts on
trade in wild Psittacus parrots, with volumes of trade
following the EU ban being substantially lower than in
the preceding two decades. It is possible that these
restrictions on imports played a role in accelerating
the expansion of the captive-breeding industry in
South Africa, which saw relatively small spikes in
imports following actions by the United States and
European Union. In addition to being used as breeding
stock, wild-sourced parrots were laundered through
South Africa where they were illegally re-exported as
‘captive-bred’(Mulliken 1995). Levels of nest poaching
of wild parrots in the Neotropics declined significantly
following US restrictions on wild bird imports, suggest-
ing that for this region, at least, the restrictions did not
simply result in a redirection of all trade to other
regions or underground (Wright et al.2001).
CITES measures, many of which were recom-
mended as part of the RST process, also appear to
have had a major influence on patterns of reported
trade, although the timing of some of these recommen-
dations makes their impact on overall levels of trade
difficult to distinguish from unilateral import bans
(CITES 2012a). While the general shift from West
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Africa to Central Africa in the mid-1990s may have
been in response to phase one of the RST, the removal
of the United States as a market for Psittacus parrots
from West Africa was likely also significant; in the
period prior to the adoption of the US Wild Bird
Conservation Act, US imports accounted for 46% of
all Psittacus parrots exported from West Africa. The
recommendations of the RST, which focused on key
exporters in West Africa, may have played a role in
limiting the degree to which exports from West Africa
reoriented to other regions, with the two regulatory
changes effectively acting in concert. However, there
are indications that in some instances these recommen-
dations, which are generally specific to particular coun-
tries, had the result of diverting trade to other areas; for
example, declines in exports from Mali and Ghana in
the late 1980s and early 1990s were offset by a rise in
exports from nearby countries (CITES 2012a). These
shifts were likely facilitated in part by the movements
of key actors to other countries in the region, with
some field studies reporting that trappers and traders
moved to other countries following localised trade
restrictions and declining populations (McGowan
2001; Annorbah et al.2016). The trade networks estab-
lished as a result of these movements may be critical in
promoting continued trade throughout the region. The
recent arrest of a Ghanian national operating in
Cameroon who was exporting parrots via West
African countries highlights the resulting complexity
of transnational trade networks (Drori in litt.toC.
Senni).
The large number of range states for Psittacus par-
rots, and the porous nature of many of the national
borders that connect them, means that there is con-
siderable potential for trade restrictions for specific
countries to simply displace trade to other areas.
Similarly, the existence of export quotas from some
countries can provide routes to international markets
for parrots illegally trapped in neighbouring countries.
The need for a coordinated regional approach to the
regulation of trade in Psittacus parrots has long been
recognised (Dändliker 1992a; Van der Heijden 2003).
Regional plans have been developed for other CITES-
listed species (e.g. Sturgeon (Acipenseriformes)) but,
despite multiple efforts, including an EU-funded work-
shop in 2013 involving multiple range states, with the
specific aim of developing synergy towards regional
management (CITES 2013b), a regional management
plan for the species is still lacking. Increased coopera-
tion between CITES Parties remains vital and it is
critically important that, following the reservations
taken to the Appendix I listing of the species in 2016
(by the DRC, Saudi Arabia and the UAE), CITES
Management Authorities of importing and exporting
countries work together to ensure that any ongoing
exports do not impact wild populations.
Commitments to not import wild-sourced Psittacus
parrots, made by the UAE and Saudi Arabia in July
2017 at the Twenty-ninth meeting of the CITES
Animals Committee, are an important step towards
this goal.
The extent to which the trade patterns reported
here, based on figures reported to CITES, reflect true
flows of trade is unclear, and the difficulties in measur-
ing levels of illegal activity are a major challenge to the
management of trade (Phelps et al.2010; Challender
and MacMillan 2014; Solomon et al.2015; Hinsley
et al.2016). Investigations of legally reported trade
can provide some insight into aspects of illegal trade,
and the patterns described in this study suggest some
areas for further investigation. Increased imports of
significant volumes of captive-bred and wild-sourced
parrots into countries bordering the European Union,
including Serbia and Turkey (Figure 2(c), country
codes RS and TR) suggest that these countries may be
operating as conduits for illegal trade into EU coun-
tries. This suggestion is further supported by a number
of recent seizures of Psittacus parrots entering Bulgaria
and Hungary, and a 2013 undercover investigation
detailing the role of Turkey in imports of wild-sourced
parrots from the DRC into the European Union (C.
Senni pers. comm.). In Singapore, discrepancies in
reported imports and exports suggest that significant
levels of unreported trade may exist (Poole and
Shepherd 2017). Poole and Shepherd (2017) further
noted that local markets were unlikely to be able to
absorb the large numbers of parrots being imported
into Singapore, and emphasise the need for improved
monitoring and reporting of trade, notably of (re-)
exports to Taiwan which is not a Party to CITES.
Some unusual and apparently illogical trade patterns
of re-exports have also emerged in recent years, includ-
ing re-exports of reportedly captive-bred parrots from
Mali and the complex web of trade among countries in
the Arabian Peninsula, where regional internal trade of
captive-bred parrots originating from South Africa has
frequently occurred. Between 2007 and 2014 these
exports have involved 17 652 specimens, with trade
reported to have occurred in opposing directions
between several trading partners in several years.
Exports of reportedly captive-bred Psittacus parrots
from the UAE have even been reported into South
Africa recently despite the flow of tens of thousands
of captive-bred parrots in the opposite direction (de
Greef 2016). These flows of parrots are particularly
worthy of greater scrutiny given the recent rise to
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prominence of the Arabian Peninsula as a market for
Psittacus parrots, and the fact that the UAE and Saudi
Arabia entered reservations for the Appendix I listing
and have imported significant quantities of wild-
sourced birds from the DRC. Although listing in
CITES Appendix I may reduce opportunities for illegal
trade through such routes, further investigations, vigi-
lance by border authorities and the careful develop-
ment of policies (e.g. on registration of Psittacus
parrots within the European Union) are vital to ensure
that illegal trade does not occur at unsustainable levels.
The relationship between trade in wild and captive-
bred Psittacus parrots also demands further scrutiny.
While theory suggests that bringing to market large
quantities of affordable, high-quality captive-bred spe-
cimens could lessen illegal collection of wild specimens
and drive down market prices (Bulte and Damania
2005), the circumstances under which such interven-
tions may be effective are lacking empirical study
(Sutherland et al.2009; Phelps et al.2014). Trade
patterns observed in this study suggest that the links
between markets for captive-bred and wild-sourced
Psittacus parrots are complex and the outcomes of
policy interventions difficult to predict. Although it is
possible that captive-bred production has served to
offset rising demand in parts of Asia, imports of wild-
sourced parrots into Western Asia have increased in
recent years in spite of massive rises in captive-bred
imports from South Africa. The reasons for this
increase deserve further investigation, although several
potential explanations exist, including the possibility
that increased availability of Psittacus parrots in mar-
kets in the region has stimulated demand, and that
wild-sourced parrots are being imported as breeding
stock for locally based captive-breeding operations to
supply domestic demand.
While captive-bred parrots are widely held to make
better pets than wild ones, the degree to which captive-
sourced Psittacus parrots are readily substitutable for
wild-sourced parrots in some markets is unclear. The
efficacy with which large quantities of Psittacus parrots
can be trapped in the wild and their low rates of
reproduction in captivity mean that wild birds are
cheaper to obtain and as a result markets may exist
among ill-informed and less wealthy consumers.
Captive-breeding operations in South Africa have also
historically imported wild-sourced birds as breeding
stock and, despite exporting over 20 000 parrots a
year in the late 2000s, South Africa was also the largest
importer of wild-sourced Psittacus parrots. The poten-
tial for the avicultural industry in South Africa to
achieve the recent massive increase in exports of ‘cap-
tive-bred’Psittacus parrots is unclear and warrants
further investigation. Between 2013 and 2014 exports
rose by 56%, a 27 604 increase. Given the current
enormous scale of the parrot-breeding industry in
South Africa (Russo 2015), substantial opportunities
exist for the laundering of wild-sourced parrots as
captive-bred breeding stock or labelled as ‘captive-
bred’for export, and it is critical that steps are taken
to ensure that the industry is adequately regulated and
compliant with CITES. There is a need to adopt robust
systems for marking and tracking parrots, including
the use of closed rings on all parrots bred in captivity
and lockable rings in combination with subcutaneous
microchip transponders for those already in captivity.
The establishment of a central repository of blood
samples from all parrots would allow for analysis of
parentage, as has been recently discussed for other
parrots in South Africa (Coetzer et al.2017). Detailed
record keeping by breeders should be accompanied by
frequent and unannounced checks on breeding facil-
ities and of shipments at the point of export.
Furthermore, the use of wild-sourced breeding stock
should be phased out to ensure that breeding opera-
tions are self-sustaining. Imports of purportedly cap-
tive-bred parrots into South Africa should be
scrutinised closely.
The transfer of the species to Appendix I of CITES
requires that breeding facilities wishing to export
Psittacus parrots must register with CITES. At present
no taxon-specific CITES guidelines exist for the regis-
tration and inspection of parrot-breeding facilities,
such as those produced for reptiles in South-eastern
Asia (TRAFFIC 2013). The production of such guide-
lines would be timely and should be given careful
consideration. The development of effective regulation
of captive-breeding operations should also consider
how the benefits of the trade are shared between
CITES Parties. Increased restrictions on wild-sourced
exports have reduced the potential for range states to
benefit from the trade, possibly reducing incentives to
manage wild populations sustainably. Consideration
should be given to the development of mechanisms
for sharing the benefits derived from captive breeding,
such as a levy on exports from non-range states direc-
ted towards capacity building and conservation.
Conclusions
Despite numerous interventions aimed at controlling
trade, declines in wild populations of Psittacus par-
rots are increasingly well documented (Martin et al.
2014; Annorbah et al.2016; Hart et al.2016).
Although it is too early to know whether the recent
listing of Psittacus parrots in Appendix I of CITES
10 R. O. MARTIN
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will be effective at reducing the exploitation of wild
populations to sustainable levels, numerous opportu-
nities for illegal trade such as poor compliance with
quotas, mislabelling of specimens and the use of
fraudulent permits will be eliminated. It is critical
that strategies for controlling complex and dynamic
trade in wildlife use a multifaceted approach and are
based on robust information about the drivers of
trade and its impacts on wild populations (Phelps
et al.2014;Challenderet al.2015). Numerous knowl-
edge gaps currently exist and there is a need for
research to understand factors that affect the supply
and demand of wild parrots, the scale and nature of
illicit trade, the links between captive-bred and wild-
sourced markets, the factors that undermine govern-
ance at national and sub-national (e.g. provincial)
levels, and the potential for growth in demand for
Psittacus parrots within Africa, which is currently
relatively small. Enforcement measures against the
trafficking of wild-sourced birds for breeding stock
and as pets should be accompanied by market-based
interventions such as targeted demand-reduction
campaigns aimed at changing consumer behaviour.
As one of the most traded exotic pets listed under
CITES (Bush et al.2014), the challenges of control-
ling the trade in Psittacus parrots are numerous and
success will be achieved only through regional colla-
boration in implementing a carefully considered,
multifaceted strategy.
Acknowledgements
I would like to thank Cristiana Senni, Ann Michels, Jamie
Gilardi, Steve Beissinger, Sue Lieberman and an anonymous
reviewer for technical advice and comments which greatly
improved the manuscript.
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