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Global wildlife trade is financially lucrative, frequently illegal and increases the risk for zoonotic disease transmission. This paper presents the first interdisciplinary study of Vietnam's illegal wild bird trade focussing on those aspects which may contribute to the transmission of diseases such as Highly Pathogenic Avian Influenza (HPAI) H5N1. Comparing January 2009 data with that of May 2007, we found a five-fold increase to 9,117 birds on sale in Hanoi. Ninety-five percent of Hanoian bird vendors appear unaware of trade regulations and across Vietnam vendors buy birds sourced outside of their province. Approximately 25% of the species common to Vietnam's bird trade are known to be HPAI H5N1 susceptible. The anthropogenic movement of birds within the trade chain and the range of HPAI-susceptible species, often traded alongside poultry, increase the risk Vietnam's bird trade presents for the transmission of pathogens such as HPAI H5N1. These results will assist in the control and monitoring of emerging zoonotic diseases and conservation of Southeast Asia's avifauna.
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EcoHealth
Conservation Medicine: Human
Health:Ecosystem Sustainability Official
journal of International Association for
Ecology and Health
ISSN 1612-9202
Volume 8
Number 1
EcoHealth (2011) 8:63-75
DOI 10.1007/s10393-011-0691-0
Investigating Vietnam’s Ornamental Bird
Trade: Implications for Transmission of
Zoonoses
Kelly Edmunds, Scott I.Roberton, Roger
Few, Simon Mahood, Phuong L.Bui,
Paul R.Hunter & Diana J.Bell
1 23
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Investigating Vietnam’s Ornamental Bird Trade: Implications
for Transmission of Zoonoses
Kelly Edmunds,
1
Scott I. Roberton,
2
Roger Few,
3
Simon Mahood,
4
Phuong L. Bui,
5
Paul R. Hunter,
6
and Diana J. Bell
1
1
Centre for Ecology, Evolution and Conservation, University of East Anglia, Norwich NR4 7TJ, UK
2
Wildlife Conservation Society, Vietnam Program, PO BOX 179, Hanoi, Vietnam
3
Overseas Development Group, School of International Development, University of East Anglia, Norwich NR4 7TJ, UK
4
Fauna and Flora International, 340 Nghi Tam, Hanoi, Vietnam
5
Centre for Natural Resources and Environmental Studies, Vietnam National University, 19 Le Thanh Tong, Hanoi, Vietnam
6
Faculty of Medicine and Health Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Abstract: Global wildlife trade is financially lucrative, frequently illegal and increases the risk for zoonotic
disease transmission. This paper presents the first interdisciplinary study of Vietnam’s illegal wild bird trade
focussing on those aspects which may contribute to the transmission of diseases such as Highly Pathogenic
Avian Influenza (HPAI) H5N1. Comparing January 2009 data with that of May 2007, we found a five-fold
increase to 9,117 birds on sale in Hanoi. Ninety-five percent of Hanoian bird vendors appear unaware of trade
regulations and across Vietnam vendors buy birds sourced outside of their province. Approximately 25% of the
species common to Vietnam’s bird trade are known to be HPAI H5N1 susceptible. The anthropogenic
movement of birds within the trade chain and the range of HPAI-susceptible species, often traded alongside
poultry, increase the risk Vietnam’s bird trade presents for the transmission of pathogens such as HPAI H5N1.
These results will assist in the control and monitoring of emerging zoonotic diseases and conservation of
Southeast Asia’s avifauna.
Keywords: bird trade, wildlife trade, Vietnam, H5N1, zoonotic disease
INTRODUCTION
The international trade in wildlife products provides ample
opportunity for the intercontinental transmission of wild-
life diseases (Daszak et al., 2000). Illegal wildlife trade poses
higher risks for disease control as animals are unlikely to be
subject to the same veterinary controls as legally traded
wildlife (Fe
`vre et al., 2006).
Over recent years, countries throughout Southeast Asia
have been significantly affected by recurrent outbreaks
of (Highly Pathogenic Avian Influenza) HPAI H5N1 virus
(Olsen et al., 2006; Thorson et al., 2006). Vietnam has reported
more HPAI H5N1 poultry outbreaks than any other country,
reportedly losing over 50 million domestic poultry as a direct
result of HPAI H5N1 infection and control (Sims and Dung,
2009). In Vietnam, birds are some of the most popularly tra-
ded species with Hanoians identifying wild birds as being the
most common live wild animal purchased (Drury, 2009).
HPAI H5N1 transmission risk factors include exposure at live
Published online: August 2, 2011
Correspondence to: Kelly Edmunds, e-mail: k.edmunds@uea.ac.uk
EcoHealth 8, 63–75, 2011
DOI: 10.1007/s10393-011-0691-0
Original Contribution
Ó2011 International Association for Ecology and Health
Author's personal copy
bird markets (Mounts et al.,1999;Wangetal.,2006); close
interactions with poultry and the preparation of poultry for
consumption (Bridges et al., 2002; Dinh et al., 2006). At least
one fatal human infection with H5N1 has been linked to live
bird markets leading to the banning of the sale of wild birds in
H5N1 hotspots (Wang et al., 2006).
When wild birds are traded, they are in contact with
many other species before being shipped to markets, sold
locally or released into the wild through religious practices
(Karesh et al., 2005). Hunters, wholesale traders and con-
sumers all experience some form of contact with each
animal passing through the trade system. These factors,
combined with the growing incidence of emerging infec-
tious disease (EID) events and the capacity of viruses such
as HPAI viruses to cross species boundaries, identifies the
wildlife trade as a key driver in the transmission and spread
of EIDs.
In the early 1990s, birds from Vietnam were reported
in increasing numbers across Southeast Asia’s markets
(Nash, 1994). More recent surveys of live bird markets
within Vietnam’s capital of Hanoi indicated that the caged
bird trade had been escalating up to 2003 (Morris, 2001;
Franklin, 2005). However, a 2007 study found a decline in
the number of birds on sale and this was attributed to
legislation introduced by the Vietnamese government in
2005 (Decree 69/2005/TT-BNN; Brooks-Moizer et al.,
2008). This legislation, issued by the central Vietnamese
government, details the restrictions put in place to limit the
spread of HPAI H5N1 and includes a total ban on the
transportation and sale of wild birds and ornamental birds
across all of Vietnam’s urban areas. Despite this ban, the
trade in ornamental birds still occurs openly across Viet-
nam’s cities.
This paper investigates the scale of the ornamental bird
trade within Vietnam with particular focus on the charac-
teristics of the trade which may contribute to the trans-
mission of diseases such as HPAI H5N1. We report on the
current extent of Hanoi’s wild bird trade, the species being
exploited and their IUCN (International Union for Con-
servation of Nature) threatened status. We describe the first
surveys of ornamental bird shops in Hue and Da Nang
cities and in Tinh Gia (Thanh Hoa province), as well as
surveys in Hanoi and Ho Chi Minh City (HCMC) and
compare the trade across these locations. Vendors were
interviewed to determine the reasons that certain taxa are
selected for purchase, their awareness of regulations con-
cerning the trade in ornamental birds and the origins of the
birds they sell. The potential role that these illegal markets
may play in the spread of EIDs such as HPAI H5N1 is
discussed.
METHODS
Market Surveys: Hanoi
For the purposes of this paper, we refer to an ornamental
bird market (OBM) as an area in which vendors sell wild
birds from permanent shops. Several such markets had
been identified during previous surveys (Morris, 2001;
Franklin, 2005; Brooks-Moizer et al., 2008) and these were
visited in October 2008 to determine whether OBMs were
still operating.
From November 2008 to February 2009 monthly sur-
veys were conducted in all known OBMs across Hanoi.
During these surveys, one or two experienced surveyors
counted the number of individuals of each bird species in
every shop within each market. Due to the illegal nature of
the trade, this information was recorded into a concealed
dictaphone. All taxa were identified to species-level where
possible with the exception of the three Munia species
(White-rumped Munia Lonchura striata, Scaly-breasted
Munia L. punctulata and Chestnut Munia L. atricapilla),
two Bushlarks (Indochinese Bushlark Mirafra erythrocep-
hala and Australasian Bushlark M. javanica) and two
White-eye species (Oriental White-eye Zosterops. palpe-
brosus and Japanese White-eye Z. japonicus) which were
grouped as Munia spp., Bushlark spp. and White-eye spp.
respectively. The Munias were typically seen in mixed-
species cages of up to 300 birds/cage making species-level
counts very difficult, whilst the White-eye species are dif-
ficult to identify to species-level during such surveys. Any
unknown species were described into the dictaphone and
where possible, photos were taken to facilitate identifica-
tion through the use of bird identification guides (Robson,
2005; Nguyen et al., 2005) and consultation with local
ornithologists. The larger markets have particular days,
related to the lunar calendar, which are believed to be lucky
for the purchase of special items such as ornamental birds
and trees. Whenever possible the surveys took place on
consecutive days each month with at least one of the days
for each survey coinciding with the special lunar calendar
days (Survey 1—10th, 11th, 13th November 2008; Survey
2—22nd, 23rd, 29th December 2008; Survey 3—18th, 19th,
23rd January 2009; Survey 4—18th, 19th February 2009).
Any shops which were closed on one day were visited again
as soon as possible until each survey was completed.
64 Kelly Edmunds et al.
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Market Surveys: Outside Hanoi
Ornamental bird shops in the cities of HCMC, Hue and Da
Nang and Tinh Gia town (Thanh Hoa province) were also
surveyed (Fig. 1). The location of these shops outside
Hanoi was determined by asking local people, bird keepers,
internet searches for related newspaper articles and reports
and liaison with conservation NGOs and staff from Saigon
(HCMC) zoo. The methodology replicated that used in
Hanoi’s shops. Surveys in HCMC took place on the 7th and
8th January 2009; in Hue on the 11th February 2009; in Da
Nang on the 1st and 2nd December 2008 and in Tinh Gia
on the 11th December 2008 and 11th February 2009. For
logistical reasons each shop was surveyed once.
Vendor Interviews
With the help of a Vietnamese field assistant, all known
vendors operating from permanent premises in Hanoi,
HCMC, Hue, Da Nang and Trinh Gia were asked if they
would answer a standard set of questions about their trade.
Semi-structured interviews were conducted with
co-operating vendors. The interview questions (see
Appendix 2 for example questionnaire) sought to deter-
mine (a) how the arrival of HPAI H5N1 in Vietnam had
affected their trade, (b) if income diversification methods
had been employed by vendors during HPAI H5N1 out-
breaks, (c) how the ornamental bird trade had changed
since HPAI H5N1 arrived in Vietnam, (d) if selling orna-
mental birds was the main source of income for vendor
households, (e) consumer preferences of species and spe-
cies’ characteristics, and lastly (f) if vendors were aware of
any regulations concerning the sale of ornamental birds.
Research involving human participants received ethical
approval from the University of East Anglia’s international
development research ethics committee. All interviews were
recorded using a dictaphone and following the interviews
the recordings were transcribed by both members of
the interview team. During extraction, the data were
made anonymous and the original dictaphone recordings
destroyed.
Figure 1. Map of Vietnam and
neighbouring countries showing
the five cities visited during 2009
surveys of Vietnam’s ornamental
bird trade.
Bird Trade and Zoonoses in Vietnam 65
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Statistical Analysis
Market Surveys
Mann–Whitney U-tests were used to compare (a) the
number of birds available for sale in different cities across
Vietnam, (b) the proportion of the trade made up of
captive-bred species in 2007 and 2009.
The species communities within the OBMs in each of
the areas surveyed were compared for similarity using
pairwise ANOSIM (analysis of similarity) using the soft-
ware PRIMER-e (Clarke and Gorley, 2006).
RESULTS
Comparing the Ornamental Bird Trade in Hanoi
Across Years
During our 2008/09 surveys, we visited the same six mar-
kets identified during previous surveys (Morris, 2001;
Franklin, 2005; Brooks-Moizer et al., 2008) as well two
shops not previously located. In total seven OBMs were
surveyed with a total of 40 shops. At any one time, the
maximum number of shops selling ornamental birds in
Hanoi was 38, with two shops sometimes only selling bird
cages or pet food and no ornamental birds. Twenty five of
the 38 (65.7%) shops in the January 2009 surveys sold
poultry alongside ornamental birds, typically keeping fewer
than 20 birds in cages adjacent to the ornamental bird
cages. Our surveys recorded a maximum of 9,117 indi-
viduals of 43 species in January 2009.
Taking into account the species known to be susceptible
to HPAI H5N1 (Appendix 1) and assuming no bird is in
stock for longer than 1 month, of the 36,584 birds counted
across all of the 2008/09 Hanoi surveys, 28,158 (77%) were
known to be HPAI H5N1-vulnerable species. Of the 66
species identified to species-level in Hanoi, 91% (60/66) are
classed as species of Least Concern (LC) on the IUCN Red
List 2009, with just one species (1.5%) from a threatened
category (Appendix 1). Four species were identified by ven-
dors as being primarily captive-bred namely Canaries,
Spotted Doves, Java Sparrows and Budgerigars (Fig. 2).
Comparing the Ornamental Bird Trade Elsewhere
in Vietnam
Seven permanent shops and two mobile vendors were sur-
veyed in HCMC, seven permanent shops in Hue, 14 semi-
permanent shops (each shop is always in the same place but
are roadside stalls as opposed to permanent buildings) in
Tinh Gia and two permanent shops in Da Nang.
In total, at least 69 species were recorded across Viet-
nam’s OBMs during the 2008/09 surveys, including the
three Munia spp. and three other taxa which were not
identified to species-level (White-eye spp., Phylloscopus
warbler spp. and Lark spp.). The composition of species
making up the trade varied across locations (Fig. 3). In
particular, the species composition in Tien Gia was highly
Figure 2. The ten most common
species recorded during a survey of
Hanoi’s ornamental bird shops in
January 2009 and the correspond-
ing numbers of those species
recorded during previous surveys.
* Denotes a species reported by
ornamental bird vendors to be
captive-bred. Data sourced from
Morris 2001 (2000 and 2001),
Franklin 2005 (2003) and Brooks-
Moizer et al.2008 (2007).
66 Kelly Edmunds et al.
Author's personal copy
dissimilar to that in all other markets (R>0.7, Table 1).
Species composition in Hanoi was similar to both Da Nang
and Hue, whereas Ho Chi Minh City was moderately dis-
similar to Hanoi and Da Nang (Fig. 3; Table 1). Hue was
intermediate between Ho Chi Minh City and Hanoi. The
most diverse markets in terms of species richness and
abundance were seen in Hanoi with the least diverse for
species richness and abundance being those in Da Nang
and Hue, respectively (Fig. 3; Table 1).
More birds were available for sale within shops in
Hanoi than in all other cities surveyed (mean number
species per shop ±S.E, Hanoi 11.27 ±1.02; outside
Hanoi 7.88 ±0.614, Mann–Whitney U-test, U = 348.5,
P= 0.012, n= 66).
Vendor Perceptions
Of the 33 ornamental bird vendors operating within
Hanoi’s six markets during the December 2008 surveys, 20
agreed to be interviewed (60.6% response rate). Both of the
vendors operating in Da Nang (100%), six of the seven
vendors in Hue (85.7%), eight of the 14 vendors in Tinh
Gia (57.1%) and six of the seven vendors HCMC (85.7%)
also agreed to be interviewed.
Selling birds was cited as the main source of income
for the households of 21 of the 42 vendors (50%) and a
key income source for a further ten vendors (23.8%).
Twenty seven of the 42 respondents (64.3%) were selling
birds when HPAI H5N1 was first reported in Vietnam in
2003. Four vendors (9.5%) started their ornamental bird
business since the introduction of Decree 69/2005/TT-
BNN in 2005.
Of the 27 vendors selling birds when Decree 69/2005/
TT-BNN was introduced, 22 (81.5%) reported having to
stop selling birds for a period of time as a result of HPAI
H5N1. Despite the legislation banning the trade in orna-
mental birds still being in effect, the modal time period
which vendors reported ceasing to sell birds was
3–6 months with one vendor choosing to stop selling birds
permanently. Of the 16 vendors in Hanoi who reported
having to stop selling birds due to a ban, six (37.5%)
reported that they resumed selling birds when the Gov-
ernment ‘‘told them that they could.’’
Within Hanoi, one vendor stated that he was aware of
some restriction on which birds they could sell but was
unable to say which birds this covered. The remaining 19
vendors stated that they were not aware of any restriction
or regulations concerning which birds they could sell.
Twelve of the 22 vendors (54.5%) outside Hanoi had some
knowledge of the restrictions regarding the sale and
transportation of ornamental birds.
All 37 of the vendors responding to questions regard-
ing the source of their birds, reported buying birds sourced
outside of the province where the birds were being sold.
Thirty four of the vendors (92%) reported buying birds
from several different areas. Three of the eight vendors in
Figure 3. The ordination plot showing the relative similarity to each
other, of the species assemblages within ornamental bird shops at five
localities across Vietnam. The surveyed shops within each location
are represented by individual symbols. Points clustered closer
together are more similar in their species composition than those
presented further apart. ANOSIM results; Global R=0.557,
P=0.001.
Table 1. RValues from ANOSIM (Analysis of Similarity) Pairwise Tests Comparing Species Composition and Evenness Across Or-
namental Bird Markets in Different Cities of Vietnam
City Hanoi Ho Chi Minh Da Nang Hue
Ho Chi Minh 0.491**
Da Nang 0.186 0.453*
Hue 0.173 0.088 0.688*
Tien Gia 0.78** 0.7** 0.856* 0.763**
** Denotes significant to the 0.001 level, * denotes significant to the 0.05 level.
Bird Trade and Zoonoses in Vietnam 67
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Tinh Gia named the provinces in which their birds were
caught as Nghe An, a neighbouring province with moderate
forest cover. Eight of the 42 vendors (19%) across Vietnam
reported that the number of ornamental bird suppliers has
increased since before bird flu reached Vietnam. Four
vendors reported an ability to supply species at our request,
providing we ‘‘order’’ in advance.
DISCUSSION
Our surveys found that since 2007, the ornamental bird
trade in Hanoi has increased in terms of the number of
individuals exploited by the trade. Bird markets in Hanoi
stock more birds than elsewhere in Vietnam and also
contain the highest diversity of species. A number of the
species common to Vietnam’s bird trade are known to be
susceptible to HPAI H5N1 and this, combined with the
large proportion of shops which sell poultry alongside
ornamental birds and the distances over which birds are
transported, increases the risk that the country’s orna-
mental bird trade may provide a mode of transmission for
HPAI viruses. Ninety-five percent of Hanoian bird vendors
stated that they were unaware of restrictions on the birds
they can sell. Selling ornamental birds is a main source of
income for the household’s of almost three-quarters of the
vendors questioned.
Trade Volume
The volume of the ornamental bird trade in Hanoi has
changed significantly with a five-fold increase in the
number of birds being recorded in January 2009 compared
to previous surveys in May 2007. The number of species
and individuals recorded in the Hanoi shops in January
2009 was similar to the pre-HPAI H5N1 levels seen in the
2003 (Franklin, 2005) surveys. When comparing our sur-
veys with those from 2007 (Brooks-Moizer et al., 2008)we
find increases of 387 and 5% in the number of individuals
and species, respectively (Fig. 2).
It has been estimated that 60% of birds caught in the
wild perish before international exportation (In
˜igo-Elias
and Ramos, 1991). Up to 36,584 birds were counted across
the 2008/09 Hanoi surveys and taking into account birds
which die before reaching the markets and those which are
exported internationally, this is likely to underestimate the
overall number of birds extracted from the wild. Despite
the increase in trade volume seen in Hanoi, the number of
species seen only increased by 5%. Seasonality is unlikely to
account for the changes seen in the species composition of
the trade across years as the most common species in the
trade are species resident to Vietnam.
Trade Across Vietnam
We found very few threatened taxa in Vietnam’s OBMs
(one species of 69, 1.4%) which does not reflect their
representation amongst the country’s native avifauna in
which around 10% of the 822 species are classified in IUCN
threatened categories (Warne and Tran, 2002; BirdLife
International, 2008). This raises questions about how or if
Vietnam’s threatened bird species are being traded. Ven-
dors reported being able to acquire less commonly traded
birds at a customer’s request so it is likely that they are
present within the trade network. Two possible explana-
tions are that the country’s rarer birds are being traded out
of Vietnam, perhaps by air, land or sea, or that they are not
displayed openly within the shops. A study of the wildlife
trader network in Quang Tri province, central Vietnam
identified ten bird species being caught for the wildlife
trade, five of which were not seen in any of our surveys
across Vietnam (Mahood et al., 2008), suggesting there may
be local, rather than wide-scale, demand for these species.
Investigations in the northern Vietnamese province of
Quang Binh found 74 wildlife traders, 23 of whom reported
trading internationally with the remainder supplying the
cities of Hanoi and Vinh (Roberton, 2004). In our survey,
one vendor in Tinh Gia reported that Chinese buyers often
visit his stall to buy birds to then transport by road to
China. The same vendor also reported having friends who
collect birds from Malaysia and Lao PDR for him to sell. It
may be the case that the more difficult to source and
probably more expensive of Vietnam’s birds are being
routed to China and other Southeast Asian countries via
the well-developed international illegal wildlife trade net-
works.
Surveys in the mid-1990s found 18 shops in HCMC
and 13 in Hanoi (Nash, 1994), whereas our surveys
15 years later found a shift to four-times as many OBMs in
Hanoi compared to HCMC. Shops in Vietnam’s capital city
of Hanoi contained more individuals for sale than the
68 Kelly Edmunds et al.
Author's personal copy
shops elsewhere in the country as well as the highest species
diversity. Species diversity was second highest in Vietnam’s
most populous city (GSO, 2008), Ho Chi Minh, with
diversity in the markets of Tinh Gia, along the main
highway to Hanoi, also relatively high. These three loca-
tions all have excellent road access to other areas of Viet-
nam as well as to other countries (by road to China, to Lao
PDR from Tinh Gia and to Cambodia from HCMC).
Hanoi and HCMC also both have international airports
and HCMC has international trade links with Cambodia
via the Mekong River. A combination of varied trade routes
and high human population densities is likely to promote
the diverse ornamental bird trade seen in these locations.
The species composition of ornamental birds on sale varied
across Vietnam and that on sale in Tinh Gia differed from
that recorded at all other locations. Transport links, trade
networks, consumer preferences and proximity to forest are
likely to be the main factors driving these differences across
localities.
The majority of live ornamental birds within the trade
are reportedly sourced directly from the wild either as free-
flying adults or as nestlings with captive breeding only
being the major source for relatively few species namely
budgerigars Melopsittacus undulates, cockatiels Nymphicus
hollandicus, canaries Serinus canaria, some finch species
and most Agapornis lovebirds (Beissinger, 2001). On the
Indonesian islands of Java and Bali, the popular practice of
keeping ornamental birds as pets and for singing contests is
threatening the long-term future of many songbird species
(Jepson and Ladle, 2005; TRAFFIC, 2008). The popularity
of this practice in Indonesia has seen an increase in the
number of songbird breeders and these owners breed a
number of threatened and non-threatened species in cap-
tivity (TRAFFIC, 2008). Only one of Hanoi’s ornamental
bird vendors reported breeding birds themselves and it is
likely that the captive breeding of these birds takes place in
the households of non-vendors.
Bird Shops and Disease Transmission
The government legislation (Decree 69/2005/TT-BNN)
introduced to regulate the trade of wild and ornamental
birds also includes clauses which ban the raising of poultry
in urban areas as well as restrictions on the sale of poultry
from infected areas and poultry known or suspected to be
infected with an HPAI virus. Almost two-thirds of the
shops surveyed in Hanoi in February 2009 sold poultry
(primarily chickens, occasionally guinea fowl) alongside
ornamental birds providing an optimal environment for
the mixing of pathogens via direct contact or airborne
transmission. Live bird markets in Hong Kong and Paki-
stan have previously been shown to contain HPAI H5N1
positive species (Promed Mail, 2007a,b,2008). Cages
within Vietnam’s OBMs are typically crowded with con-
specifics and stacked on top of, and next to, cages con-
taining other species. This arrangement contributes
towards a stressful captive environment for the birds as well
as promoting pathogen transmission both between and
within species. The number of birds seen in the Hanoi
surveys alone known to be susceptible to HPAI H5N1, the
mixing of poultry and ornamental birds within Vietnam’s
OBMs, and the subsequent sale and transportation of these
birds, suggest that these ornamental bird shops could
contribute to the perpetuation and spread of pathogens
such as HPAI H5N1.
Trade Controls and Legislation
To control the impact that the ornamental bird trade may
have on pathogen transmission and wild bird populations,
effective control measures need to be developed. Trade
bans require enforcement and an understanding of local
livelihood dynamics to be able to apply effective trade
controls (Cooney and Jepson, 2006). In Vietnam, this
would necessitate enforcement and promotion of the
existing legislation by a law-abiding enforcement agency
coupled with education for bird vendors willing to adhere
to any legislation. Legislation introduced in 2005 in an
attempt to control the spread of HPAI H5N1 was suggested
as responsible for the decline in the ornamental bird trade
recorded in Hanoi in the 2007 survey (Brooks-Moizer et al.,
2008) but the scale of the trade has expanded since then
despite the law still being in effect. Knowledge of the
existing legislation and bird-related pathogen risks varies
across the country. Over half of the vendors operating
outside of Hanoi have some knowledge of the restrictions
on their trade but only one of Hanoi’s 20 responding
ornamental bird vendors reported knowledge of or pre-
tended to be aware of regulations. None of the Hanoi’s
vendors reported the police confiscating any of their birds.
We witnessed the police in Hanoi confiscating ornamental
birds from mobile vendors who were operating their
Bird Trade and Zoonoses in Vietnam 69
Author's personal copy
business on the pavement and, according to the police
this was because the vendors were causing an obstruction
for pedestrians. The fate of the confiscated birds is
unknown.
Currently, there is little other evidence that existing
legislation is being enforced and due to the cultural
importance and value associated to keeping ornamental
birds in Vietnam, a new approach is required if this trade is
to be regulated and the risks of pathogen transmission
minimised. The vendors’ ability to move and hide their
birds at short notice, as exhibited during the early HPAI
H5N1 outbreaks in Vietnam (Edmunds et al. In prep)
highlights the problems of controlling this trade and the
disease threats it may pose.
CONCLUSION
We propose that the effective control of Vietnam’s orna-
mental bird trade requires increased awareness and
enforcement of legislation integrated with a programme of
health surveillance for the live bird markets. Such a scheme
would allow for effective monitoring of the markets
alongside confiscations of illegal animals whilst also
introducing a regular screening programme for the legally
traded (primarily captive-bred) species already present
within the trade system.
This is the first comprehensive study of Vietnam’s
illegal wild bird trade and we hope its results may inform
effective control and monitoring of zoonotic EIDs and the
conservation of Southeast Asia’s avifauna.
ACKNOWLEDGMENTS
The authors thank the Economic and Social Research
Council (ESRC), the Natural Environment Research
Council (NERC) and Newquay Zoo Environmental Park
for financial support. KE was funded by ESRC/NERC
studentship ES/F009925/1. We also thank the Centre for
Natural Resources and Environmental Studies in Hanoi for
providing logistical support.
APPENDIX 1
See Table 2.
Table 2. The Number of Individuals for the 68 Species Recorded During Surveys of Wild Bird Markets Across Vietnam.
Number of shops: Market
IUCN status Hanoi (Nov) Hanoi (Dec) Hanoi (Jan) Hanoi (Feb) HCMC Hue Tinh Gia Da Nang
34 33 37 34 9 7 14 2
Species
Columbiformes
Barbary Dove Streptopelia roseogrisea LC 16 6 35 428
Emerald Dove Chalcophaps indica LC 1
Eurasian Collared Dove Streptopelia decaocto LC 14 8 9
Spotted Dove*
a
Streptopelia chinensis LC 315 332 363 515 9 8 60 8
Coraciiformes
Dollarbird Eurystomus orientalis LC 1
Cuculiformes
Asian Koel Eudynamys scolopacea LC 1
Greater Coucal Centropus sinensis LC 3
70 Kelly Edmunds et al.
Author's personal copy
Table 2. continued
Number of shops: Market
IUCN status Hanoi (Nov) Hanoi (Dec) Hanoi (Jan) Hanoi (Feb) HCMC Hue Tinh Gia Da Nang
34 33 37 34 9 7 14 2
Falconiformes
Black Baza Aviceda leuphotes LC 1
Galliformes
Common Pheasant*
b
Phasianus colchicus LC 8
Passeriformes
Baya Weaver Ploceus phillipinus LC 223
Black Bulbul*
c
Hypsipetes leucocephalus LC 18
Black-collared Starling*
d
Sturnus nigricollis LC 10 6 4 3 1
Blue Magpie*
e
Urocissa erythrorhynca LC 1262
Black-naped Oriole*
f
Oriouls chinensis LC 1 2
Black-throated Laughingthrush Garrulax chinensis LC 381 463 389 338 41 40 90 8
Blue-winged Leafbird Chloropsis cochichinensis LC 2
Blue-winged Minla Minla cyanouroptera LC 1
Bushlark spp. Mirafra spp. 13 2
Common Green Magpie Cissa chinensis LC 1
Common Myna*
d
Acridotheres tristis LC 45 17 7 2 12 1 5 2
Common Tailorbird Orthotomus sutorius LC 15
Crested Myna*
g
Acridotheres cristatellus LC 35 11 8 4 1 12
Eurasian Tree Sparrow*
c
Passer montanus LC 4 1 2 12
Golden-fronted Leafbird Chloropsis aurifrons LC 11
Great Tit Parus major LC 4 3 12 1
Greater Necklaced Laughingthrush Garrulax pectoralis LC 7
Hill Myna*
f
Gracula religiosa LC 52 42 54 33 8 4
Hwamei Garrulax canorus LC 357 724 720 722 17 6 5 3
Island Canary Serinus canaria LC 165 190 208 223 4 2
Java Sparrow Padda oryzivora VU 1 1 1 10
Leafbird spp. Chloropsis spp. LC 3 3 2
Lesser Necklaced Laughingthrush Garrulax monilegur LC 3 8 7 38 40
Light-vented Bulbul Pycnonotus sinensis LC 1
Munia 3 spp.*
e,g
(known for two of these spp.) Lonchura spp. LC 1753 2327 4337 3860 25 790
Oriental Magpie Robin*
a
Copsychus saularis LC 69 118 94 142 65 18 3 1
Paddyfield Pipit Anthus rufulus LC 44 24 12 6 4 1 1 1
Bird Trade and Zoonoses in Vietnam 71
Author's personal copy
Table 2. continued
Number of shops: Market
IUCN status Hanoi (Nov) Hanoi (Dec) Hanoi (Jan) Hanoi (Feb) HCMC Hue Tinh Gia Da Nang
34 33 37 34 9 7 14 2
Phylloscopus warbler spp. Phylloscopus spp. 41
Pied Bushchat Saxicola caprata LC 1 1 2 5
Red Avadavat Amandava amandava LC 29 36 27 8 10
Red-billed Leiothrix*
f
Leiothrix lutea LC 276 213 208 41 2
Red-billed Starling*
g
Sturnus sericeus LC 1 2 26
Red-whiskered Bulbul*
d
Pycnonotus jocosus LC 614 705 875 731 42 150 237
Rufous-cheeked Laughingthrush Garrulax castanotis LC 3
Rufous-vented Laughingthrush Garrulax gularis LC 1 2
Scarlet-backed Flowerpecker Dicaeum cruentatum LC 5
Siberian Rubythroat Lusciana calliope LC 2
Silver-eared Mesia*
e
Leiothrix argentauris LC 70 82 7 34
Stripe-throated Bulbul Pycnonotus finlaysoni LC 1
Vietnamese Greenfinch Carduelis monguilloti NT 1
Vinous-breasted Starling Sturnus burmannicus LC 1
White-crested Laughingthrush Garrulax leucolophus LC 1 5 4 1 10 1 23
White-eye 2 spp.*
e
Zosterops spp. 2527 1962 1200 1250 45 34 14 1
White-rumped Shama Copsychus malabaricus LC 51 167 56 51 27
White-shouldered Starling Sturnus sinensis LC 10 78
White-vented Myna*
a
Acridotheres grandis LC 2 2
Zebra finch*
h
Taeniopygia guttata LC 2553
Piciformes
Blue-throated Barbet Megelaima asiatica LC 1111
Psittaciformes
Alexandrine Parakeet Psittacula eupatria LC 1 1 3 1
Blossom-headed Parakeet Psittacula roseate LC 3
Budgerigar*
h
Melopsittacus undulatus LC 634 315 179 348 146 23 5
Cockatiel Nymphicus hollandicus LC 35 9 40 19
Fischer’s Lovebird/Lovebirds spp. Agapornis spp. NT 92 68 69 82 5
Grey-headed Parakeet Psittacula finschi LC 21 6 9
Red-breasted Parakeet Psittacula alexandri LC 122 37 169 81 38 1 7
72 Kelly Edmunds et al.
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APPENDIX 2: AN EXAMPLE OF THE QUESTIONS
ASKED TO ORNAMENTAL BIRD VENDORS
DURING A SURVEY OF VIETNAMS
ORNAMENTAL BIRD TRADE IN 2009
Market Interviews
Interview date: Market: Shop #:
Interviewee age: Gender:
Questions
1. How long have you been selling live birds?
2. Which are the five most popular species? Does this
change throughout the year?
3. Why are these species preferred?
4. Which species are the most profitable? Is this always
the same?
5. What are the main reasons why people buy birds?
6. Is there a large supply of birds for you to buy for your
shop?
7. Do you breed any birds yourself?
8. Where do the birds you sell come from? Are they from
close to the city or another province?
9. Are the birds you sell captive-bred (farmed) or wild-
caught?
10. Is selling birds your household’s primary source of
income?
11. How is the trade in birds now compared to other years?
12. When there is little demand for birds, how do you
replace the lost income?
13. Have you ever had to stop selling birds? Why?
14. Are there any shops which used to sell birds but no
longer do? Do you know why they stopped selling
birds? What do they now sell?
15. Have there been any confiscations of birds from this
market? Who by? What did they confiscate? When? Why?
16. Have the health department bought any of your birds?
17. How has your business been affected by bird flu?
18. How long did bird flu affect your business?
19. Do you perceive yourself to be at risk from bird flu?
20. Do you take any precautions to prevent the transmis-
sion of bird flu to yourself or your birds?
21. Are there any regulations regarding the birds which you
can sell? Are any species restricted/prohibited to sell?
22. Were there any laws introduced to try and control bird
flu?
23. Do any of your customers buy birds to take overseas?
Table 2. continued
Number of shops: Market
IUCN status Hanoi (Nov) Hanoi (Dec) Hanoi (Jan) Hanoi (Feb) HCMC Hue Tinh Gia Da Nang
34 33 37 34 9 7 14 2
Total species 47 35 35 37 28 18 21 12
Total individuals 7769 7907 9117 9017 567 321 395 1059
*Indicates that HPAI H5N1 infection has been reported for that species. Italics denote a species that is unique to the markets in that area. The IUCN statuses of the species are shown and represent LC least
concern, NT neat threatened and VU vulnerable (IUCN, 2010).
a
Siengsanan-Lamont et al. (2010).
b
Perkins and Swayne (2001).
c
Kou et al. (2009).
d
Siengsanan-Lamont (2010).
e
Promed-Mail (2007).
f
Promed-Mail (2005).
g
Smith et al. (2006).
h
Perkins and Swayne (2003).
Bird Trade and Zoonoses in Vietnam 73
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Bird Trade and Zoonoses in Vietnam 75
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... These differences in cultural and historical backgrounds suggest that the composition and origins of species in the bird trade may differ between geographic regions Edmunds et al., 2011;Jepson & Ladle, 2005;Severinghaus & Chi, 1999). ...
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... Finally, if geographical factors were important, we would expect alien species to be more likely sourced from neighboring countries of the studied market because these species should be more available for trade (Chng et al., 2015;Edmunds et al., 2011;Gilbert et al., 2012;Nijman, 2010;Shepherd, 2006). Thus, we should not expect similarities in species shared among the three markets due to their disparate locations. ...
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The IPBES Bureau and Multidisciplinary Expert Panel, in the context of the extraordinary situation caused by the COVID-19 pandemic, and considering the role that IPBES can play in strengthening the knowledge base on biodiversity, decided that IPBES would organize a “Platform workshop” on biodiversity and pandemics, in accordance with the procedures for the preparation of IPBES deliverables, in particular decision IPBES-3/3, annex I, section 6.1. on the organization of Platform workshops. This workshop, held virtually on 27-31 July 2020, provided an opportunity to review the scientific evidence on the origin, emergence and impact of COVID-19 and other pandemics, as well as on options for controlling and preventing pandemics, with the goal to provide immediate information, as well as enhance the information IPBES can provide to its users and stakeholders in its ongoing and future assessments. This workshop report supports IPBES Plenary-approved activities, and is considered supporting material to authors in the preparation of ongoing or future IPBES assessments, and, in particular, in the preparation of the scoping report for a future thematic assessment of the interlinkages among biodiversity, water, food and health (decision IPBES-7/1, II). The workshop brought together 22 experts from all regions of the world, to discuss 1) how pandemics emerge from the microbial diversity found in nature; 2) the role of land-use change and climate change in driving pandemics; 3) the role of wildlife trade in driving pandemics; 4) learning from nature to better control pandemics; and 5) preventing pandemics based on a “One Health” approach. The workshop participants selected by the IPBES Multidisciplinary Expert Panel included 17 experts nominated by Governments and organizations following a call for nominations and 5 experts from the ongoing IPBES assessment of the sustainable use of wild species, the assessment on values and the assessment of invasive alien species, as well as experts assisting with the scoping of the IPBES nexus assessment and transformative change assessments. In addition, resource persons from the Intergovernmental Panel on Climate Change (IPCC), the Secretariat of the Convention on Biological Diversity (CBD), the Secretariat of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), the United Nations Convention to Combat Desertification (UNCCD) and the World Health Organization (WHO) attended the workshop. This workshop report has been prepared by all workshop participants and been subjected to several rounds of internal review and revisions and one external peer review process. Technical support to the workshop has been provided by the IPBES secretariat. IPBES thanks the Government of Germany for the provision of financial support for the organization of the workshop and production of the report.
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The Convention on the International Trade in Endangered Species of Wild Fauna and Flora (CITES) is the most important global initiative to monitor and regulate the international trade of plants and animals, but there is a lack of (retrospective) assessments of the effectiveness of its actions. We here focus on the international trade in Chinese hwamei Garrulax canorus, a songbird native to south-eastern China and northern Lao PDR and Vietnam. Prior to the year 2000, the species was heavily traded as an ornamental cage bird, both in countries within and outside its natural range. In an effort to prevent international overexploitation, at the request of China, the Chinese hwamei was listed in Appendix II of CITES, regulating all international trade. Here we compare data from three non-range countries (Thailand, Singapore and Indonesia) for which we have bird market survey data prior to and following the CITES listing. In addition, we assess whether or not CITES import and export figures agree with observations in the bird markets, and explore the contemporary (online) trade and trafficking in Chinese hwamei. We find a clear effect of the CITES listing and Chinese export restrictions in Indonesia (before ∼50 birds / survey vs ∼15 birds / survey after), but not in Thailand (∼10 vs ∼13) and Singapore (∼4 vs ∼16). Singapore is the only country that reports the import of Chinese hwamei, 1,650 birds in 2002-2004 only, possibly accounting for a proportion of the birds observed in trade. In contrast, neither Thailand nor Indonesia report the import of a single Chinese hwamei since its CITES listing, despite some 2,000 birds having been recorded openly for sale, suggesting large-scale illegal international trade in the species. Five seizures in Singapore and Indonesia were mostly because of concern about avian influenza. Price data, corrected for inflation, suggests that prices for Chinese hwamei have increased substantially, albeit following a delay, from ∼US$50 prior to the listing to ∼US$200 after. We conclude that the CITES Appendix II listing of Chinese hwamei has had some positive effect on reducing the volumes of these birds in international trade, mainly through implementation of domestic legislation in China, but that substantial illegal or undocumented trade persists in Southeast Asia, involving organised criminal networks. We recommend actions from range countries, such as China, to cease the illegal export of Chinese hwamei, from importing countries such as Indonesia, to ensure no illegal shipments of birds enter their country, and for consumer countries where the species cannot legally be traded to curb the illegal domestic trade as the demand for songbirds in these markets drives the trafficking.
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A considerable variety of Indonesian avifauna is forced into the domestic and international pet trade, where the majority of individuals are caught in the wild. To monitor the volume and development of the trade and to evaluate the threat status of the traded species, bird market surveys are usually performed. The most commonly used monitoring technique is the “Direct Counting Method – DCM”, i.e. the counting of openly displayed individuals offered for sale. In this study, we evaluate the reliability of the outputs that DCM delivers by conducting regular long-term bird censuses at two of the main animal markets in Medan (Sumatra, Indonesia) involving 10 major local vendors specialising in the Sumatran Laughingthrush ( Garrulax bicolor ; SL), our target species. Both markets were visited from March to December 2015 with three different survey intervals (one, two and four visits per month). In total, according to DCM, we recorded up to 461 SL individuals offered for sale. However, a comparison of the monthly logs recorded directly by the vendors during the same period revealed that DCM only uncovered a negligible proportion of the total trade. Specifically, we detected only 4.6%, 8.1% and 16.1% of the traded SL individuals in relation to the set survey intervals. While the numbers of recorded SL individuals according to DCM and the three survey intervals were significantly interrelated, none of them correlated with the real numbers of traded birds provided by the vendors. Our results suggest that census-based market data are underestimated, and represent an unknown proportion of true trade volumes, regardless of the intensity of visits. In order to obtain reliable data and prevent the underestimation of the volume of trade, we recommend of undisclosed monitoring of markets and the engagement of trusted individuals with a past personal interest in this field or, if possible, the vendors themselves.
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Wildlife trade and emerging infectious diseases pose significant threats to human and animal health and global biodiversity. Legal and illegal trade in domestic and wild birds has played a significant role in the global spread of highly pathogenic avian influenza H5N1, which has killed more than 240 people, many millions of poultry, and an unknown number of wild birds and mammals, including endangered species, since 2003. This 2007 study provides evidence for a significant decline in the scale of the wild bird trade in Hanoi since previous surveys in 2000 (39.7% decline) and 2003 (74.1% decline). We attribute this to the enforcement of Vietnam's Law 169/2005/QD UBND, introduced in 2005, which prohibits the movement and sale of wild and ornamental birds in cities. Nevertheless, 91.3% (21/23) of bird vendors perceived no risk of H5N1 infection from their birds, and the trade continues, albeit at reduced levels, in open market shops. These findings highlight the importance of continued law enforcement to maintain this trade reduction and the associated benefits to human and animal health and biodiversity conservation.
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Bird-keeping is an extremely popular pastime in Indonesia, where there is a thriving internal market in both wild-caught and captive-bred birds. However, little is known about whether the scale of bird-keeping represents a genuine conservation threat to native populations. Here we present the results of the largest ever survey of bird-keeping among households in Indonesia's five major cities. Birds were found to be urban Indonesia's most popular pet (kept by 21.8% of survey households) and we conservatively estimate that as many as 2.6 million birds are kept in the five cities sampled. Of bird-keeping households, 78.5% kept domestic species and/or commercially bred species and 60.2% kept wild-caught birds that we classified into three conservation categories: native songbirds, native parrots and imported songbirds. Compared to non-bird owners, households keeping wild-caught birds in all three conservation categories were richer and better educated, whereas households owning commercially-bred species were richer but not better educated and households keeping domestic species did not differ in educational or socio-economic status. We conclude that bird-keeping in Indonesia is at a scale that warrants a conservation intervention and that promoting commercially-bred alternatives may be an effective and popular solution.
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The outbreak of highly pathogenic avian influenza of the H5N1 subtype in Asia, which has subsequently spread to Russia, the Middle East, Europe, and Africa, has put increased focus on the role of wild birds in the persistence of influenza viruses. The ecology, epidemiology, genetics, and evolution of pathogens cannot be fully understood without taking into account the ecology of their hosts. Here, we review our current knowledge on global patterns of influenza virus infections in wild birds, discuss these patterns in the context of host ecology and in particular birds' behavior, and identify some important gaps in our current knowledge.
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Markets for endangered species potentially generate incentives for both legal supply and poaching. To deter poaching, governments can spend on enforcement or increase legal harvesting to reduce the return from poaching. A leader-follower commitment game is developed to examine these choices in the presence of illegal harvesting and the resulting impacts on species stocks. In addition, current trade restrictions imposed under the Convention on International Trade in Endangered Species of Wild Fauna and Flora are examined. With Cournot conjectures among poachers, the model details the subgame perfect equilibrium interactions between poaching levels, enforcement and legal harvesting. Copyright Australian Agricultural and Resource Economics Society Inc. and Blackwell Publishing Ltd 2004.
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A serological and virological surveillance program to investigate the HPAI H5N1 virus in wild bird populations was undertaken from February 2007 to October 2008. The purpose of the survey was to investigate the infection status in free ranging wild birds in Banglane district, Nakhon Pathom province, central Thailand. Samples from wild birds were collected every two months. Choanal and cloacal swabs, serum and tissue samples were collected from 421 birds comprising 44 species. Sero-prevalence of the virus tested by H5N1 serum neutralization test (using a H5N1 virus clade 1; A/chicken/Thailand/vsmu-3-BKK/2004) was 2.1% (8 out of 385 samples; 95% CI 0.7, 3.5). Species that were antibody positive included rock pigeons (Columba livia), Asian pied starling (Gracupica contra), spotted dove (Streptopelia chinensis), oriental magpie robin (Copsychus saularis), blue-tailed bee-eater (Merops philippinus), myna (Acridotheres spp.), and pond heron (Ardeola spp.). Prevalence by H5N1 virus isolation was 0.5% (2 out of 421 samples; 95% CI 0.0, 1.1); the two H5N1 virus-positive samples were from Asian pied starling (Gracupica contra) and white vented myna (Acridotheres grandis). Positive virological samples were collected in June 2007 while all positive serology samples were collected between May and August except for one sample collected in December 2007. No positive samples were collected in 2008. Molecular studies revealed that the wild bird H5N1 viruses were closely related to poultry viruses isolated in other parts of Thailand. However, there was no poultry H5N1 prevalence study performed in the study site during the time of this wild bird survey. Interpretation of source of virus isolates would include spill-over of H5N1 viruses from contaminated sources due to movement of domestic poultry and/or fomites from other areas; or infection of wild birds within the outbreak locations and then translocation by wild bird movement and interaction with wild birds inhabiting distant locations.