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Biological Conservation 243 (2020) 108431

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

It's in the news: Characterising Indonesia's wild bird trade network from T
media-reported seizure incidents

Karlina Indraswaria, , Rachel S. Friedmanb, Richard Noskec, Chris R. Shepherdd, Duan Biggse,f,g,h,
Connie Susilawatia, Clevo Wilsona
a
School of Economics and Finance, QUT Business School, Brisbane 4000, Australia
b
School of Earth and Environmental Sciences, University of Queensland, St. Lucia, Brisbane, Australia
c
Centre for Biodiversity and Conservation Science, University of Queensland, St. Lucia, Brisbane, Queensland 4072, Australia
d
Monitor Conservation Research Society, Box 200, Big Lake Ranch, B.C., Canada
e
Environmental Futures Research Institute, Griffith University, Nathan, Brisbane, Queensland 4111, Australia
f
ARC Centre of Excellence for Environmental Decisions, Centre for Biodiversity & Conservation Science, School of Biological Sciences, University of Queensland, St. Lucia,
Brisbane, Queensland 4072, Australia
g
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
h
Centre for Complex Systems in Transition, School of Public Leadership, Stellenbosch University, Stellenbosch 7600, South Africa

A R T I C LE I N FO A B S T R A C T

Keywords: Devising strategic conservation plans to curb Indonesia's wild bird trade is pivotal to protect species. However,
Bird trade, Indonesia limited understanding of nation-wide trade network patterns could hinder this urgently necessary action.
Trade network Currently, available information either have restricted geographical scope or is focused on trans-national ana-
Songbirds lysis, limiting understanding of domestic-level nation-wide spatial movement and patterns of traded birds. In this
Parrots
paper, we use media-reported local seizures to understand patterns in a domestic-level wild bird trade network.
Cockatoos
Indonesia's bird trade network involved 18 countries (including Indonesia), all 34 provinces, and 132,945
confiscated birds from 157 species. Songbirds (Passeriformes) (83.8% of all birds) dominated the trade, with the
highest number of birds in demand for songbird competitions and listed as of conservation concern in the IUCN
Red List. The most important region and the main transit point was Jakarta, the most important source of birds
was Lampung and the most important destination for birds was West Java. Malaysia was the most important
international source of songbirds (mostly smuggled into Indonesia), while the Philippines was the main inter-
national destination for the smuggling of Parrots and Cockatoos. Seizures mostly occur near transit and desti-
nation regions, and fewer near source regions. Despite the identified patterns, it is likely a small portion of the
actual size of Indonesia's bird trade. This paper provided a low-cost approach for a rapid wildlife trade network
analysis and could be easily used to identify trade patterns of other taxa in other countries.

1. Introduction competitions (Burivalova et al., 2017; Eaton et al., 2015; Iskandar and
Iskandar, 2015). Most of the millions of birds traded in Indonesia an-
The wildlife trade devastates species populations (Nijman et al., nually are predicted to have been harvested from the wild in an un-
2018; Ribeiro et al., 2019; Ribeiro et al., 2019; Sodhi et al., 2016, 2008; sustainable manner causing a rapid population decline for many of
Symes et al., 2018). This is particularly apparent in countries where the Indonesia's native bird species (Bergin et al., 2017; Harrison et al.,
domestic market for wildlife is present due to high demand, high 2016; Jepson and Ladle, 2009; Rentschlar et al., 2018). In 2018, In-
profitability and cultural acceptance (Hinsley et al., 2018; Nyaki et al., donesia's government revised its list of protected species and, in the
2014; Ribeiro et al., 2019). Indonesia is an example of such a country case of songbirds, increased the number of protected species to 557
(Burivalova et al., 2017; Jepson and Ladle, 2011). Bird keeping has species. However, three months prior to the release of this law, pro-
made the bird trade highly lucrative, with the presence of active mar- tection over five highly harvested species was rescinded due to lobbying
kets country-wide and the rise of economically profitable songbird by songbird communities (Chng et al., 2018a, 2018b; Leupen et al.,


Corresponding author at: Business School Queensland University of Technology, Z Block, QUT Gardens Point Campus, 2 George St, Brisbane 4000, Australia.
E-mail addresses: karlina.indraswari@hdr.qut.edu.au (K. Indraswari), r.friedman@uq.edu.au (R.S. Friedman), rnoske@tpg.com.au (R. Noske),
chris.shepherd@mcrsociety.org (C.R. Shepherd), d.biggs@griffith.edu.au (D. Biggs), c.susilawati@qut.edu.au (C. Susilawati), clevo.wilson@qut.edu.au (C. Wilson).

https://doi.org/10.1016/j.biocon.2020.108431
Received 17 June 2019; Received in revised form 1 January 2020; Accepted 23 January 2020
0006-3207/ © 2020 Elsevier Ltd. All rights reserved.
K. Indraswari, et al. Biological Conservation 243 (2020) 108431

2018; Mongabay, 2018). The communities believed that the population Nijman, 2018). Seizure news reports have also been used for a global
of bird species currently owned and traded are not under threat due to assessment of ivory trade, which resulted in conservation actions and
the presence of breeding practices. However, information on In- further demand reduction (Underwood et al., 2013).
donesia's bird populations in the wild and those that have entered the In this study we explore the breadth of information that can be
trade are currently limited to certain locations and are not available provided by news reported seizures to assess: 1) patterns present in
nation-wide (Chng and Eaton, 2016; Harris et al., 2015; Marshall et al., Indonesia's bird trade routes, 2) identify hotspot regions of high priority
2019; Nijman et al., 2017). This restricts the ability to gauge the true and 3) assess whether current confiscation efforts have optimally ad-
size of unsustainable trade. Evidence to assess whether Indonesia's dressed areas of main concern. This research is then used to highlight
harvest of wild birds is bringing about a rapid population decline na- the urgency for conservation action in response to what is reported to
tion-wide is therefore urgently required. be a rampant bird trade in Indonesia. This research focuses on the bird
The bird trade trend in some countries is similar to that of trade in Indonesia but could generally be applied to trade route analysis
Indonesia, the domestic trade is potentially a larger contributor to bird of other countries given regular reporting in news sources on con-
population declines compared to trans-national trade (Berkunsky et al., fiscation of wildlife. Domestic level analysis of the bird trade that covers
2017; Martin, 2018; Pires, 2012). Similarly, as for Indonesia, informa- several species and a wide spatial scope is pivotal to provide informa-
tion to support this assumption and understand the true extent of the tion for policy formulation, program implementation and conservation
domestic bird trade is often lacking (Ribeiro et al., 2019). This hinders strategies aimed at protecting species and curbing illegal and un-
strategic planning to deliver rapid and optimal response needed to sustainable trade.
protect species. Commonly used to measure the extent of wildlife trade
and its trade routes are publicly available databases (Challender et al., 2. Materials and methods
2015; Heinrich et al., 2016; Patel et al., 2015; Ribeiro et al., 2019).
However, extractable information available from these databases are 2.1. Study site
usually heavily reliant on English-based sources and are focused on
trans-national trade (Patel et al., 2015; Ribeiro et al., 2019). Some Indonesia consists of 34 provinces and has the fourth highest
databases provide information limited to certain geographical regions. number of bird species in the world, with 1777 recorded species, of
Information from the Convention on International Trade in Endangered which 515 are endemic (BurungIndonesia, 2018). A total of 30 species
Species (CITES) of Wild Fauna database for example, is limited to sig- are listed by the International Union for Conservation of Nature (IUCN)
natory countries and is dependent on different levels of reporting efforts Red list as critically endangered (CR), 48 species as endangered (EN),
of its members (Phelps et al., 2011; Ribeiro et al., 2019; Siriwat and 93 species as vulnerable (VU), 243 species as near threatened (NT), and
Nijman, 2018). Similarly, work done using the UN Office on Drugs and 11 species as data deficient (DD). Indonesia has the world's second
Crime's World Wildlife Seizures Database (UNDOC WISE) and highest number of globally threatened species (Birdlife, 2019; IUCN,
HealthMap database provide an analysis at trans-national level, with 2019), and currently, as many as 557 species are currently listed in
only limited domestic level data (Patel et al., 2015). Data could po- Indonesia's protected species list (KLHK, 2018).
tentially be acquired from non-government organisations (NGOs) and
government organisations (Challender et al., 2015): but these data are 2.2. Data collection
often scattered and could entail complicated methods to organise in a
common data base as well as difficulties in obtaining multiple usage Data on media-reported bird seizures were obtained from online
permissions. These limitations potentially make data gathering to fa- news articles published over a 10-year period. Data collected were
cilitate a crucially important understanding of the numerous inputs into seizures that occur between 1 January 2010 to 13 November 2019,
the domestic-level wildlife trade, a difficult task. Published work on using the Google News search engine. Searches were carried out
market surveys, interviews and assessment of expert opinions are al- iteratively in three-month periods, until the selected keywords (in both
ternative approaches which can be used to understand a country's do- English and Indonesian) detected several media reported seizures
mestic trade, yet for such approaches to be conducted for several taxa during the search period. The keywords “Indonesia bird trade”
and on a nation-wide level is likely to be a very costly process. More- (Perdagangan Burung), “Indonesia bird smuggling” (Penyelundupan
over, given countries with a high level of domestic trade tend to be Burung), “Indonesia bird seizure” (Penyitaan Burung/ Sita Burung),
those with a high biodiversity but limited resources for research, spe- “Confiscating bird” (Amankan burung) and “Indonesia bird police/
cies protection and conservation is problematic. Therefore, to comple- natural resources agency enforcement” (Polisi burung/BKSDA burung)
ment currently available information, a low-cost approach is needed were most effective. A maximum of 20 Google search result pages per
which can deliver a reasonably rapid acquisition of information which three-month period were scanned, and items on bird seizures in
covers several species and with a large spatial distribution. Indonesia were recorded. The news source that contained most details
There has been an increasing use of local news reports on wildlife was used as the main source and was cross-checked with at least two
seizures to acquire the patterns of a country's domestic wildlife trade other sources to ensure consistent reporting. When two sources con-
and/or wild-harvested resources (Challender et al., 2015; Cheng et al., tained different information, the method that was used to obtain data
2017; Nijman, 2015; Rosen and Smith, 2010; Siriwat and Nijman, was listed in the “Data extraction” phase.
2018). Local news on seizures - either written in the local language or in
English - commonly provides valuable information on trade routes and 2.3. Data extraction
traded species at domestic levels (Hansen et al., 2012; Nijman, 2015).
Some concerns arise from the usage of such sources for data analysis, Extracted data were used to identify (1) the regions involved in the
such as the dependency on reporting rates and the potential for in- trade route and (2) the volume of birds confiscated at, originating from,
accuracy and bias in the reporting. Hence data extraction needs to be transiting through or destined for each region. For regions involved in
carried out systematically and is coupled with cross-checking from the trade route, they were considered as part of the trade route when a
multiple reporting agencies, these risks can be reduced (Nijman, 2015; confiscation occurred in the region and/or when a media report men-
Siriwat and Nijman, 2018). Seizure news reports have successfully tioned it as an origin, destination or transit location of a bird seizure
provided a deeper understanding of trade dynamics, mapped trade incident involving Indonesia or its provinces. Regions identified were
routes and identified the source, transit and destination hotspots at categorised into national (i.e. Indonesian provinces) or trans-national
domestic level for tigers (Stoner et al., 2016), pangolins (Challender (i.e. other countries), and the transportation route for each seizure in-
et al., 2015; Cheng et al., 2017) and Siamese rosewood (Siriwat and cident was mapped. For each species confiscated, they were first

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K. Indraswari, et al. Biological Conservation 243 (2020) 108431

categorised into three main order groups: songbirds (Passeriformes), network (Faggini et al., 2019; Halkos and Tsilika, 2017). In this study, a
parrots and cockatoos (Psittaciformes), and other orders. They were region was made equivalent to a node, and the node's connectivity was
then classified into the most specific taxa information available. When measured through a region's centrality values (Borgatti et al., 2009).
articles did not mention a bird taxon, species were recorded as “birds” Three centrality values were used: in-degree centrality (which measures
only. Such recordings were included to identify the volume of con- the number of incoming connections), out-degree centrality (the
fiscated birds throughout the search period but were excluded from number of outgoing connections) and betweenness centrality (the
order-based analyses. number of transit connections).
The volume of birds traded were recorded according to the number Social network analysis maps networks from a single connection by
mentioned in identified articles. Occasionally there would be articles connecting two nodes with an incoming and outgoing connection.
mentioning confiscated birds but with only vague indications of value. Information on wildlife transportation routes may involve more than
If the numbers of birds differed between articles on the same seizure, one connection, therefore for this analysis, shipments were broken
the number was averaged and rounded down, while referring to the down into single connections to allow connections to be measured se-
main article for other details. If there was no mention of the number of parately. For example, a shipment that travelled from Jambi to Jakarta
traded birds, the volume was listed as one. If an approximate number with a transit connection in Lampung, would be broken down into two
was mentioned, the volume was listed as the lowest value of that ap- connections: one between Jambi (origin location with an outgoing
proximation. For example, if the article mentioned “hundreds”, the connection) and Lampung (a destination location with an incoming
volume was listed as “100”, and thousands as “1000”. When the taxa connection), and one between Lampung (now the origin location with
were mentioned but number of birds were not, to allow inclusion of an outgoing connection) and Jakarta (a destination location with an
analysis the bird was listed as one. When only the total number of birds incoming connection). A more detailed explanation of how shipment
was mentioned, and the group consisted of several taxa, the volume of connections were measured and mapped can be found in Patel et al.
birds was divided equally among the identified birds in the group. This (2015). After connectivity were identified and centrality values mea-
number was then used for the analysis. However, the number is not sured, patterns that emerge from identified connections between nodes
listed as the recorded volume of bird species listed in the supplementary were clustered using the Walktrap algorithm (Pons and Latapy, 2006)
material. with a maximum of a 5-path connection between nodes. This meant
All identified bird species were checked for their conservation status that nodes that had tendency to have a connection between each other
and population status in the International Union of Conservation of were clustered in a single group. However these connections did not
Nature (IUCN) Red List (IUCN, 2019) and in Indonesia's protection exceed five path connections, or exceed the presence of four transit
status list based on the 2018 regulation by the Ministry of Environment nodes within a single path.
and Forestry (KLHK, 2018).
All data were recorded in English. In instances where the news ar- 2.4.3. Identification of hotspots and regions of trade network importance
ticle was in Indonesian only, the first author provided the translation For identification of hotspot regions, all centrality measures (in-
required for information extraction. degree, out-degree and betweenness) were normalised with a range
from 0 to 1 to allow comparison and minimise variation. For each
2.4. Data analysis measurement, the higher the centrality value, the higher number of
incoming, outgoing, or transit connections are present involving a node
Data analysis was carried out in three phases: (or in this case, a region). A region's activity level is based on combining
its normalised centrality measures with the normalised value for vo-
1) Species accumulation curve phase which assessed the likelihood of lume of birds that are shipped with each seizure incident (the volume of
the addition of species along with the addition of seizure informa- birds seized was normalised to the range 0 to 1). The calculation of the
tion. normalised values for the hotspot areas are as follows:
2) Analysis of the trade network: mapping of trade routes and de-
termining the role of each region. Source hotspot
3) assessment of whether current confiscation efforts have optimally = (In −degree centrality+destination volume) − betweenness centrality
focused on regions at the start of the trade chain.
Sink hotspot
2.4.1. Species accumulation curve
= (Out−degree centrality+origin volume) − betweenness centrality
The species accumulation curve was created by treating every sei-
zure incident as a separate observation and analysed as to whether an
Transit hotspot = betweenness centrality
increase in seizure incidents will cause an increase in the number of
species (Ugland et al., 2003). A species accumulation curve that nears Total hotspot value = source hotspot + sink hotspot + transit hotspot
its asymptotic richness indicates that it is close to saturation and will
not increase number of observed species with increase in recorded Regions with high activity levels are considered hotspot locations.
seizure incidents. The species accumulation curve was extrapolated Measurement of the total hotspot value was carried out for all the birds
using the “random” method to achieve a closer approximation of the altogether (that is, not distinguishing order groups). The separate
curve and was fitted using a logistic approach. analysis for each order group (songbirds, parrots and cockatoos, and
other orders) can be seen in this article's supplementary material. The
2.4.2. Trade route mapping and hotspot measurement using social network total of hotspot values may exceed 1.0, potentially creating a difficulty
analysis for comparisons between regions. Therefore, values were once again
This study used social network analysis (Wasserman and Faust, normalised to create weighted values for each variable that ranged from
1994) to map Indonesia's current bird trade network. Social network 0 to 1, to facilitate comparisons. The closer the sum value is to 1, the
analysis maps a network based on the level of connectivity of each of its more important it is for the flow of Indonesia's wild bird trade network.
nodes (Freeman and White, 1991; Patel et al., 2015; Wasserman and
Faust, 1994) and has been used to identify country roles in global trade 2.4.4. Assessing efficacy of enforcement action
routes (Heinrich et al., 2016; Patel et al., 2015; Reino et al., 2017). To easily understand whether seizures of identified bird families
Social network connectivity identified in the analysis represents the have optimally been conducted in a source hotspot region, normalised
importance of a node in connecting one node to another within a values of the volume of individuals categorised into the family-level

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taxa for each seizure region were mapped out in a Non-Metric The highest proportion of bird orders involved in the trade network
Multidimensional Scaling (NMDS) ordination. An NMDS ordination were songbirds, comprising 83.8% of all confiscated birds. Parrots and
allows a clearer understanding of data through mapping it out so that cockatoos were the second most trafficked group, comprising around
the patterns of distribution emerge. An efficient seizure would be car- 5.4% of all confiscated birds and other orders comprised only 0.9% of
ried out at the location closest to its source. Therefore, regions were confiscated birds. Unidentified orders made up 9.9%. The specific
labelled based on their source hotspot values on the NMDS ordination. number of birds seized for each order can be seen in the supplementary
We iteratively performed the NMDS analysis and found that NMDS material.
performed with k = 2 and permutation = 100 was most descriptive. It The most frequently used routes and largest volume of birds trans-
was then assessed whether bird families are most likely to be seized in ported on the routes were birds from Lampung (Table 1). Forty-two
these source hotspot regions or further down the line of the transpor- routes that were recorded were used to transport birds more than once
tation chain. The source hotspot values were distinguished as follows: and 82 routes recorded were used only once. The most frequently used
1) above 0.5: very high source hotspot region; 2) 0.1–0.5: high source route was Lampung to Banten, followed by Lampung to Jakarta. The
hotspot region; 3) 0.01–0.1: moderate source hotspot region; 4) below largest volume of birds transported were from Lampung to Banten
00.1 low source hotspot region. followed by Lampung to West Java. Also frequently used import routes
All analysis was performed using the R Studio version 3.2.3. Species were from Malaysia, either to Riau Islands or West Kalimantan; from
accumulation curve and NMDS analysis was done using package Vegan Kalimantan, Sulawesi and Papua into East Java and a route from West
(Oksanen et al., 2007). Measurement of centrality was done using the Nusa Tenggara to Bali.
network package (Butts, 2008) and mapping of the trade network was
done using the igraph package (Csárdi and Nepusz, 2006). 3.1.1. Important hotspot regions in Indonesia's bird trade network
From the top 20 hotspot regions, Jakarta was found to be the most
3. Results important and was also the top hotspot transit region for Indonesia's
bird trade network. Lampung was the top source hotspot region and
3.1. Regions involved in the trade network West Java the top sink region. East Java did not have the highest value
in any of the measurements of trade importance nor did it have high
We recorded 321 seizure incidents in Indonesia that took place in 32 source hotspot values. However, it is, nevertheless, an important des-
out of its 34 provinces with at least 132,945 birds confiscated. This tination and transit region not only as an important trade route but also
study did not find seizure records for provinces North Kalimantan and as a region with the third highest hotspot value. Malaysia and Maluku
West Sulawesi. The highest volume of birds confiscated was in were identified as having negative hotspot sink values, which indicates
Lampung (Fig. 1), where 48,490 birds (36.5% of all birds) were seized, their role as origin and transit regions is more important that as a
followed by Banten (34,285 birds or 25.8%) and East Java (9080 birds destination region. Malaysia is also found to be only trans-national
or 6.8%). The highest frequency of seizures was in East Java with 61 region to be listed in the top hotspot regions. Other important regions
seizures (19% of all seizure incidents), followed by Lampung with 32 include Riau and Jambi as source regions; Banten and Central Java as
seizures (10%) and West Kalimantan with 23 seizures (7.2%). The destination region and North Sumatra and South Sulawesi as hotspot
highest average proportion of birds confiscated per single seizure was in transit regions (Table 2).
Banten (1558 birds), followed by Lampung (1515 birds) and West Nusa Transportation routes for all three orders were found to have dis-
Tenggara (995 birds). tinct patterns. First there has been an establishment of prominent

Fig. 1. Heat map of volume of birds that were confiscated in Indonesian provinces. Provinces with the top five highest volume of birds entering or exiting a region are
listed in bold with numbers written inside yellow squares. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version
of this article.)

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Table 1
Most commonly encountered route throughout the study period alongside the volume of birds transported.
Rank Route Frequency of routes Volume transported Average volume in a route

1 Lampung - Banten 13 36,816 2832


2 Lampung - Jakarta 12 9053 754
3 Malaysia - West Kalimantan 12 3638 303
4 S. Kalimantan - East Java 9 5275 586
5 Papua - East Java 8 265 33
6 S. Sulawesi - East Java 8 1754 219
7 West Nusa Tenggara - Bali 8 11,145 1393
8 Banten - Jakarta 7 18,171 2596
9 East Java - Jakarta 7 3205 458
10 South Sumatra - Lampung 7 4443 635
11 Malaysia - Riau Islands 6 7096 1183
12 Lampung - West Java 4 23,030 5758

transportation route groups centred around Jakarta, East Java and Jakarta, East Java and Yogyakarta are also found to be transit regions
Lampung. Jakarta is found to be the main entry point from Sumatra and for trans-national connections exporting birds outside of Indonesia.
East Java the entry point from other parts of Indonesia. West Java, Parrots and cockatoos have been recorded destined for Hong Kong
although having highest sink value for all regions, did not have high through Yogyakarta then Singapore; for Taiwan and Thailand through
source or transit values. Rather, West Java was frequently shown to be a Surabaya and for China and Kuwait through Jakarta. For other orders,
sink region and part of the transportation route centred around there were three main established groups of transportation, one centred
Lampung or Jakarta (Fig. 2). around Lampung and Jakarta, one around East Java and central and
The regions identified as important differed between order groups. eastern parts of Indonesia, and one around Central Java. The source
For songbirds, there are two established routes with short transporta- regions were mainly Lampung, Papua, West Papua and Maluku, with
tion connections. The first is centred around western Indonesia, with the sink regions being West Java and Jakarta. Jakarta, East Java, South
hotspots being Jakarta, Lampung, Banten and West Java (Lampung and Sulawesi and Central Java are the main transit regions (Fig. 2).
Jakarta have the same hotspot value). The second route is centred Transportation connection routes for other orders were smaller than the
around central and eastern Indonesia, with the main hotspot being East other two order groups. Transportation connection routes for songbirds
Java. For songbirds, large volumes were found to have been transported were the largest in terms of use. As well, the number of routes and
from Lampung into Java through Banten and West Java, West Nusa volume of birds transported were also largest for songbirds. Details of
Tenggara into Bali, South Kalimantan into East Java and Malaysia into the centrality and hotspot values for each order group can be accessed
West Kalimantan and Riau Islands (Table 1 for additional information in the supplementary material.
on routes). Trans-national bird trade connections found in the form of
export from Indonesia to Hong Kong and Belgium through Singapore, 3.2. Bird orders involved in the trade network
via imports from Malaysia, and from Jakarta to France, Bahrain and
Saudi Arabia (Fig. 2). We identified 62,181 individuals to species level (46.8%), 6765
For parrots and cockatoos, the most established transportation route individuals (5.1%) to genus level, 80 individuals (0.1%) to sub-family
involves source from Eastern Indonesia, transit involving Sulawesi and level and 15,305 individuals (11.5%) to family level, and 27,128 in-
trans-national export into the Philippines. Of the four hotspot provinces dividuals (20.4%) to order level. However we could not identify some
- Jakarta, East Java, Lampung and West Java - the first three are mostly 21,486 birds (16.2%). As much as 157 bird species were identified from
are transit regions for transportation routes with short route connec- the recorded seizures, although based on the species accumulation
tions. West Java and North Sumatra are the main sink regions, while curve this number would most likely increase with addition of recorded

Table 2
Top twenty regions with highest hotspot along with its source, sink and betweenness values.
Rank Region Source Sink Betweenness Hotspot value Normalised hotspot value

1 Jakarta 0.00 0.97 1.00 1.97 1.00


2 Lampung 1.00 0.37 0.15 1.51 0.77
3 East Java 0.01 0.45 0.62 1.08 0.55
4 West Java 0.06 1.00 0.00 1.07 0.54
5 Banten 0.27 0.68 0.01 0.96 0.49
6 Central Java 0.04 0.51 0.10 0.66 0.33
7 Malaysia 0.48 −0.12 0.25 0.61 0.31
8 Maluku 0.46 −0.09 0.16 0.53 0.27
9 North Sumatra 0.06 0.20 0.26 0.52 0.27
10 South Sulawesi 0.06 0.18 0.26 0.50 0.26
11 South Sumatra 0.30 0.13 0.05 0.48 0.25
12 West Nusa Tenggara 0.16 0.26 0.06 0.48 0.24
13 Bali 0.05 0.28 0.09 0.42 0.21
14 Riau 0.35 0.02 0.05 0.42 0.21
15 Jambi 0.35 0.06 0.00 0.41 0.21
16 West Kalimantan 0.16 0.15 0.00 0.32 0.16
17 Riau Islands 0.00 0.30 0.00 0.30 0.15
18 North Sulawesi 0.11 0.16 0.02 0.30 0.15
19 South Kalimantan 0.17 0.08 0.04 0.29 0.15
20 Yogyakarta 0.09 0.06 0.13 0.28 0.14

Bold text indicate the highest value for each measurement.

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Fig. 2. Identified transportation route for (a) Songbirds (b) Parrots and cockatoos and (c) Other orders.

seizures (Fig. 3). From the identified species, 47 (29%) were listed in parrots and other order groups. The family with the highest number of
the IUCN Red List as those of conservation concern; 15 (9.6%) were seized birds were old-world flycathcers (Muscicapidae). For parrots and
identified as near threatened; 13 (8.3%) as vulnerable; 10 (6.4%) as cockatoos, out of the three families identified, parrots (Psittaculidae)
endangered; 8 (5.1%) as critically endangered and one as data defi- had the highest seizure volume. For other orders Doves and Pigeons
cient. Seventy-three (46.5%) of the seized species are listed in In- (Columbidae) had the highest volume, followed by hawks and eagles
donesia's national protected list (KLHK, 2018). One species however (Accipitride), pheasants (Phasianidae) and cassowaries (Casuaridae).
was listed under a different name. The silver-eared mesia (Leiothrix Not all bids that were identified up to family level could be identified
argentauris) is listed under the scientific name of the Sumatran mesia up to species level. Songbirds had the highest proportion of birds
(Leiothrix laurinae). identified to species level (68%), while the least were parrots and
From the seized order groups, songbirds had the highest number of cockatoos (42%) (Table 3).
species of conservation concern, while parrots and cockatoos had the
highest number of species protected under Indonesia's protected species
3.3. Optimisation of seizure efforts for bird species
list. The top five families in the songbird group had a higher number of
confiscated birds than the highest rated family for both cockatoos and
The likelihood of seizures of bird families are more prominent in

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K. Indraswari, et al. Biological Conservation 243 (2020) 108431

Fig. 3. Species accumulation curve for species recorded from identified seizure incidents showing a steady increase and not nearing an asymptote.

some regions than others. Birds that are most seized in source hotspots market and network, both in terms of the domestic level trade and also
and mainly in Lampung (Table 2), are songbirds, laughingthrushes its role the regional and global trade. Previously known information
(Leiothrichidae), weavers (Ploceidae), pipits and wagtails (Mota- acquired from on the ground short term surveys (Chng et al., 2015;
cillidae), and finches (Estrildidae). Highest seizures in the second Chng et al., 2018a, 2018b; Chng and Eaton, 2016; Shepherd, 2006)
highest source hotspot region of Banten, consisted of white-eyes (Zos- recorded particularly higher numbers of bird species for sale in market
teropidae). For Central Kalimantan top seizure rates were for pheasants locations (up to more than 200 species). This study has recorded the
(Phasianidae), for South Sulawesi eagles and hawks (Accipitridae), for trade in 132,945 individual birds. However, less than half were iden-
West Papua cockatoos (Cacatuidae) and for West Kalimantan old-world tified up to species level, around 16.8% were unable to be identified at
flycatchers (Muscicapidae). Birds such as true finches (Fringilidae), all, and the remaining was identified up to order, family or genus level.
shrikes (Laniidae), old world orioles (Oriolidae), and larks (Alaudidae) The species accumulation curve shown that the number of species re-
are likely to be seized together but not in any one distinct region. While corded would most likely increase with an increase in seizure records
sunbirds (Nectariniidae), pigeons and doves (Columibdae), Tits (Par- (Fig. 3), therefore, remains species that occur in the trade however is
idae), Wablers (Cisticolidae), bulbuls (Pycnonotidae), and songbirds yet to be detected. Information acquired from existing market survey
and birds (unidentified to family level) are also likely to be seized to- results, along with results from this study are most likely a gross un-
gether, the incidence is low in source hotspot regions (Riau Islands and derstatement of the size of Indonesia's bird trade.
West Sumatra). Seizure near locations most likely as destination regions Known is that over the period which data was collected, 18 species
also occurs for thrushes (Turdidae), starlings (Sturnidae), leafbirds have undergone population declines causing up listing in the IUCN Red
(Chloropsidae), and parrots (Psittaculidae) (Fig. 4). List, and three species were not assessed until 2016, where post as-
sessment were instantly categorised as near threatened (Psittunus cya-
nurus), vulnerable (Acridotheres javanicus) and critically endangered
4. Discussion (Acridotheres melanopterus). Three species (Pycnonotus zeylanicus,
Garrulax ruffifrons and Chloropsis sonnerati) have even been up listed
The size and growth of Indonesia's bird trade and its role in the twice in the past 3 years and the blue-winged leafbird (Chloropsis co-
global trade network is an emerging concern. Analysis of patterns and chinchinensis) has been up listed from ‘near threated’ to ‘endangered’ in
trade routes acquired from seizure data can provide valuable insights a single year (IUCN, 2019). The consequence of Indonesia's bird trade
(UNODC, 2016) to an understanding of Indonesia's clandestine bird

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K. Indraswari, et al. Biological Conservation 243 (2020) 108431

Table 3
List of identified families with the highest volume of confiscated birds for each order group.
Rank Family Seized Identified birds IUCN Red List status Indonesia protection status

Number of species Proportion of seized birds CR EN VU NT Total

Passeriformes (Total) 111,431 87 68% 5 4 2 8 19 20a


1 Muscicapidae 11,940 5 99% – – – – – –
2 Cisticolidae 10,069 2 78% – – 1 1 3
3 Chloropseidae 8678 4 100% – 2 – – 2 –
4 Paridae 7353 1 1 – – – – – –
5 Nectariniidae 7298 4 4% – – – – – –
Other families 31,699 70 70% 5 2 2 7 16 13a
Mixed speciesb 27,708 –
Unidentified 6736
Psittaciformes (Total) 7149 30 42% 1 3 3 5 12 28
1 Psittaculidae 5823 20 35% – 2 1 4 7 21
2 Cacatuidae 1129 6 71% 1 1 1 1 4 6
3 Psittacidae 124 2 100% – – 1 – 1 1
Unidentified 73 – 1%
Other orders (Total) 1229 41 66% 2 3 8 2 15 26
1 Columbidae 479 5 87% 1 – 1 2 2
2 Accipitridae 213 10 76% – 1 – – 1 9
3 Phasianidae 189 7 82% – 1 1 2 4 3
4 Casuariidae 161 1 100% – – – – – 1
5 Bucerotidae 92 6 73% – – 4 4 5
Other families 95 12 53% 1 1 2 – 4 6
Mixed speciesb 8968 –
Unidentified birds 4167
Total sum 132,945

Note: Listed alongside is the number of identified bird species, the proportion of birds identified to species level for each family, its IUCN Red List status
(CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Near Threatened), and its national protected status (KLHK, 2018).
Bold text inidcate total birds of each of the measured order groups.
a
One species, the silver-eared mesia (Leiothrix argentauris) listed with the scientific name Leiotrix laurinae.
b
Birds recorded from seizures confiscating groups of birds without details of proportion.

are silent forests. The geographical scope of the trade (through the trade much as the white-rumped shama, sunbirds are said to be very attrac-
network mapped in this work) and species identified as having been tive, unique-looking and relatively cheap to buy, facilitating the growth
involved in this trade shows the high level of conservation action that is in demand (Heikal, 2017; Turut, 2012). The interest in sunbirds started
needed to combat Indonesia's rampant bird trade. within small communities and continues to grow into a competition
category of its own in songbird competitions. Similar threats exist for
4.1. Birds involved in Indonesia's bird trade members of the white-eye family (Chng et al., 2017; Heikal, 2017; Lee
et al., 2016). Said to be small, attractive and easy to care for, these birds
Several of the most seized bird families in this work are those that are frequently confiscated in seizures (see, supplementary material).
are in demand driven by presence of bird competition and communities These newly emerging trends show that potential threat may be faced
(Heikal, 2017; Turut, 2012). The records of most confiscated birds are by many bird families.
songbirds with five of the highest confiscated families those in high The trade in parrots and cockatoos – although known for many
demand for songbird competitions (Iskandar and Iskandar, 2015; Lee years - continues to be rampant, with Eastern Indonesia as the main
et al., 2016; Sano et al., 2019; Turut, 2012). The old-world flycatcher source of birds (Cahill et al., 2006; Cottee-Jones et al., 2014; Morse,
family (Muscacipiade) contains two species, the oriental magpie robin 2018; ProFauna, 2008). There is growing trend in the sale of the parrots
and the white-rumped shama which are most in demand for songbird and cockatoos order group as well as the other orders group, via online
competitions. Birds of this family have been smuggled in large numbers sale platforms (Gunawan et al., 2017; Iqbal, 2016, 2015; Krishnasamy
from Malaysia to Indonesia (Table 1) and there have also been records and Stoner, 2016a). For the species in the Hawk and Eagle family
of smuggling between other south east Asian nations (Chng and Eaton, (Accipitridae), emerging online communities has providing platforms
2016; Leupen et al., 2018) (Fig. 2). The white-rumped shama was one for the sharing of interests in these birds and thus creating further de-
of the birds which had protection rescinded in 2018 due to lobbying mand for them (Gunawan et al., 2017; Iqbal, 2016). The demand for
from songbird owner communities (Marshall et al., 2019; Mongabay, hawks and eagles is not limited to Indonesia: sales have been recorded
2018). However, seizures, market and field survey information show a outside the country with routes identified in this study showing the
rapid decline in this species caused by outsourcing and illegal smug- presence of a trans-national trade (Krishnasamy and Stoner, 2016a,
gling. Two of the top five families - the leafbirds (Chloropsidae) and 2016b). While the confiscation level has not reached that of songbirds,
Cistocolidae warblers (mainly the bar-winged prinia) – have members the volume is nevertheless at a level which generates considerable
listed in the IUCN Red List due to over harvesting (Chng et al., 2017; concern.
IUCN, 2019). There are claims of presence of active captive bred op-
erations in Indonesia for both families. However, for the leafbirds, de- 4.2. Indonesia's bird trade transportation route: both a global and domestic
spite presence of operations, captive breeding attempts has had a very concern
low success rate causing an ongoing need for parental restock of wild
harvested birds (Asosiasi Penangkar Burung Nusantara, Asosiasi Pe- Data sourced from this study identifies the presence of both global
nangkar Burung dan Unggas Indonesia, Pers.Comm., 2019). Sunbirds and domestic level trade in birds. Despite a temporary decrease in de-
(Nectariniidae), the fifth highest confiscated species, has recently mand for birds after the 2005 European ban on bird trade (Nijman,
emerged as a competition bird. Despite its singing ability not prized as 2010) and the decline of bird trade in Indonesia due to outbreak of

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K. Indraswari, et al. Biological Conservation 243 (2020) 108431

Fig. 4. NMDS ordination plotting species and regions (provinces or countries) where species would most likely be seized. The different colour and shapes indicate
importance of a region as a source hotspot, red circles indicate source region of most importance, blue triangles regions of second source importance, green squares as
third importance and plus shapes as regions of least importance. (For interpretation of the references to colour in this figure legend, the reader is referred to the web
version of this article.)

avian influenza (Shepherd, 2006), there appears to be an increase in the network, there is potential that smuggling of birds to and from In-
global supply of birds from countries in the Indo-Malay region (Reino donesia is commonly done to meet local demand and demand in these
et al., 2017). This study has identified smuggling attempts to countries countries. Smuggling route into the Philippines, mainly for parrots and
in Europe, the middle east and east Asia and into south east Asian cockatoos (Cottee-Jones et al., 2014; ProFauna, 2008), involved central
countries (Fig. 3). Two transit countries were identified, first Singapore and eastern Indonesia and was less connected to other South East Asian
that facilitates to Europe and East Asia, and second Malaysia that fa- countries. This route was relatively more direct and concerningly in-
cilitates import into Indonesia from Vietnam and Thailand, and even volved parrots and cockatoos protected by Indonesian law.
from Malaysia itself, through Riau Island and West Kalimantan This analysis shows that Jakarta remains the most important hot-
(Table 1). Singapore and Malaysia plays an important role as a transit spot. Jakarta has been known as an important destination market for
region for global illegal wildlife (Heinrich et al., 2016; Krishnasamy, Indonesia (Bergin et al., 2017; Chng et al., 2015; Nijman et al., 2018),
2016; Leupen et al., 2018; Lin, 2005). The families of wild birds iden- and in this work also has a transit hub for both domestic and interna-
tified on sale in South East Asian countries are identical to those being tional trade. Second to Jakarta, East Java has also been known to hold
confiscated and in demand in Indonesia (Eaton et al., 2017; Edmunds the role as a transit hub (Chng and Eaton, 2016; Jepson and Ladle,
et al., 2011; Su et al., 2014). Given the similarity in demand and 2005), facilitating movement of birds, mostly by sea, into Java from
identification of important transit countries in Indonesia's bird trade regions outside of Sumatra. Movement of birds into Java from Sumatra

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K. Indraswari, et al. Biological Conservation 243 (2020) 108431

is facilitated by Lampung. The largest proportion of seizures (19%) Those such as demand for sunbirds, white-eyes and hawks and eagles
occurred in East Java while the largest volume of confiscated birds was that emerged due to presence of active communities (Gunawan et al.,
in Lampung (36.5%). High levels of seizures do not indicate culpability, 2017; Iqbal, 2016; Jepson and Ladle, 2011).
rather may indicate the opposite (UNODC, 2016). Therefore, the high Domestically, actions to support bird conservation is pivotal.
proportion of seizures in East Java's and high volume of confiscated Applicaton of conservation strategies, such as habitat protection and
birds in Lampung, along with both region's important role connecting market-based conservation, should be seriously considered in countries
regions all over Indonesia with Java, indicate that birds moving un- with a highly active bird economy such as Indonesia. Additionally,
detected through these regions is most likely to be much larger than actions to increase border enforcement to prevent wildlife trade is of
what has been identified. paramount importance. This action requires support from external
The source of birds, especially those commonly used in competi- parties because resource available for wildlife protection in developing
tions, may likely shift from Sumatra. The decline of commercially im- countries are often limited. Support in resources creates positive change
portant birds populations in Sumatra due to the trade (Harris et al., in prevention of wildlife trade (Lee et al., 2005). Internationally, a call
2017) may shift supply of birds to originate from Kalimantan, West for collaborative action is pivotal. Bodies such as the IUCN songbird
Nusa Tenggara and Malaysia (Leupen et al., 2018; Rentschlar et al., group work closely in monitoring changes in regional trade patterns
2018). This has been the case for white-rumped shama,oriental magpie and help to develop collaboration in cross-boundary conservation ac-
robins and leafbirds, where, because the supplies from Java and Su- tions. Other species, such as parrots and cockatoos also warrant at-
matra are declining, white-rumped shama and oriental magpie robins tention from local government and specialists' groups to monitor trends
are being imported from Malaysia and leafbirds are increasingly and take action. Finally, information provided in this study can provide
sourced from the forest in Kalimantan (Chng et al., 2017; Leupen et al., data and parameters required for much needed strategic planning,
2018). conservation actions and program implementation to protect traded
bird species. At the rate at which Indonesia's bird trade is expanding,
4.3. Optimisation of seizure: are seizures done near locations of origin? pressure is being exerted not only on Indonesia's own biodiversity but
also global biodiversity.
Based on the NMDS Analysis (Fig. 3), seizures in Indonesia com-
monly occur in transit and destination locations. Some birds were Role of funding source
seized in Lampung, a region identified a hotspot source region. How-
ever, identification of Lampung as a source region warrants some The Indonesian Endowment Fund for Education (LPDP Indonesia)
caution and indicates slight limitations of using news reports to un- provided funding for this study.
derstand wildlife trade patterns. Data extracted from news reports is
dependent on reporting efforts of the news source outlet. Most sources Declaration of competing interest
list Lampung as the origin of shipments; yet of the birds seized in
Lampung most are likely not to have originated from the province The authors declare that they have no known competing financial
(Harris et al., 2017). These birds are most from neighbouring provinces, interests or personal relationships that could have appeared to influ-
such as Riau, Jambi and South Sumatra (Fig. 2). Riau and Jambi ence the work reported in this paper.
themselves were found as one of the source hotspots (Table 2).
Enforcement efforts for wildlife trade are often strongest at transit Acknowledgements
regions (UNODC, 2016), however, the further the bird is seized from its
habitat, the more it is of concern. Seizure of birds far from a bird's We would like to thank Jeremy Webb for assistance in the editing of
natural habitat and distribution range may cause difficulties for re-in- this manuscript. We thank Riga Anggarendra, Wilterza Nazabban,
troduction. Birds are more likely to be subjected to stress due to long Andhie Jaya Saputra, Franmuda Agung, Rizka Astari, and Lisa Nurfalah
travels, consequently increasing their mortality rate. For Indonesia in for assistance in data collection and extraction. The authors declare no
particular, the country's geographic form as an Archipelago further conflict of interest in this study. Chris Shepherd's work on unsustainable
complicates the situation, as travel stress is greatly increased in the long songbird trade in Asia is supported by Fondation Segré and Duan Biggs
trips between islands. Release of confiscated birds is often done by is supported by an Australian Research Council Discovery Early Career
authorities in forests near seizure locations to prevent high mortality Researcher Grant (DE 160101182).
rates (Bakauheni Quarantine, Pers. Comm, 2018). However, un-
calculated release efforts may risk species invasion and increase risk of Appendix A. Supplementary data
spread of disease rate (Collar et al., 2015). Conservation efforts to re-
locate species back to their natural habitats is complex and requires Supplementary material for this report comprises (1) a complete list
substantial resources to carry out. Moreover, the locality of where a of volume of outgoing bird shipments, incoming bird shipments, con-
bird is harvested is unlikely to be known as from harvest to transpor- fiscated birds, frequency of seizures, and average number of birds per
tation undergoes several middlemen and paid couriers (Wyatt, 2013). seizure for each region and bird families, (2) centrality measures for
each region and bird order groups, (3) a complete list of identified
4.4. Call for monitoring increased enforcement and action species, and (4) a list of seized bird families during the study period. A
list of the articles used for this study is available online http://dx.doi.
This study provides a methodology which can be used to analyse org/10.17632/k7z85dv53m.1. Supplementary data to this article can
trends in the seizure of a bird taxa, covering multiple species and sev- be found online at doi: https://doi.org/10.1016/j.biocon.2020.108431.
eral families. Despite some limitations in the collection and extraction
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