Science of the Total Environment 542 (2016) 411–426

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

A review on current knowledge and future prospects of organohalogen

contaminants (OHCs) in Asian birds
Naeem Akhtar Abbasi a, Riffat Naseem Malik a,⁎, Adrien Frantz b, Veerle Leontina Bernard Jaspers c
a
Environmental Biology and Ecotoxicology Laboratory, Department of Environmental Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan
b
Sorbonne Universités, UPMC Univ Paris 06, UPEC, Paris 7, CNRS, INRA, IRD, Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-75005, Paris, France
c
Environmental Toxicology, Department of Biology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• The study reviewed the levels of lega-

cy and emerging organohalogens in
Asian birds
• Regional differences of organohalogens in
Asian birds has been shown through
maps
• The study elucidated factors which af-
fects organohalogens contamination in
birds
• The study discusses the data gaps and fu-
ture perspectives of organohalogens in
Asia
• Finally, we suggested few recommen-
dations needed to be focused in future
research

a r t i c l e i n f o a b s t r a c t

Article history: The release of harmful chemicals in the Asian environment has recently increased dramatically due to rising
Received 29 July 2015 industrial and agricultural activities. About 60% of the global human population is currently living on the Asian
Received in revised form 17 October 2015 continent and may thus be exposed to a large range of different chemicals. Different classes of organohalogen
Accepted 18 October 2015
chemicals have indeed been reported in various environmental compartments from Asia including humans
Available online 3 November 2015
and wildlife, but this issue has received less attention in birds. In this article, we reviewed the available literature
Editor: Adrian Covaci on levels of legacy persistent organic pollutants (POPs) and various flame retardants (FRs) in Asian avifauna to
analyze the existing pool of knowledge as well as to identify the gaps that should be addressed in future research.
Keywords: Furthermore, we discussed the variation in levels of organohalogens based on differences in regions, trophic
Asian birds level, dietary sources and migratory behaviors of species including distribution patterns in different tissues of
Organohalogens birds. Although the mass of published literature is very low and even absent in many important regions of
Legacy POPs Asia, we deduced from the reported studies that levels of almost all classes of organohalogens (OHCs) including
Emerging FRs FRs were highest in East Asian countries such as Japan, China and South Korea, except for HCHs that were found at
Contamination
maximum levels in birds of South India. Concentrations (ng/g LW) of different OHCs in Asian birds ranged

⁎ Corresponding author.
E-mail address: r_n_malik2000@yahoo.co.uk (R.N. Malik).

http://dx.doi.org/10.1016/j.scitotenv.2015.10.088
0048-9697/© 2015 Elsevier B.V. All rights reserved.
412 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426

between bLOD (limit of detection) to 14,000,000 for polychlorinated biphenyls (PCBs), b LOD to 790,000 for
dichlorodiphenyltrichloroethane (DDTs), bLOD to 12,000 for hexachlorobenzene (HCB), b LOD to 29,000 for
hexachlorocyclohexanes (HCHs), b LOD to 47,000 for chlordanes (CHLs) and bLOD to 4600 for total cyclodienes.
Further, ranges (ng/g LW) of 1.1 to 150,000 for Co-PCBs; bLOD to 27 for polychlorinated dibenzo-p-dioxins
(PCDDs); bLOD to 45 for polychlorinated dibenzofurans (PCDFs) and 0.02 to 73 for PCDD/DFs have been reported
in Asian aves. Among emerging FRs, levels of total polybrominated diphenyl ethers (PBDEs), total dechlorane
plus (DPs) [syn and anti DPs] and hexabromocyclododecane (HBCDs) oscillated between bLOD to 134,000,
b LOD to 3820 [b 0.1–920 and b0.1–2900], and bLOD to 11,800 ng/g LW, respectively. Corresponding ranges
of novel brominated flame retardants (nBFRs) such as decabromodiphenyl ethane (DBDPE) and 1,2-bis(2,4,6-
tribromophenoxy)ethane (BTBPE) were bLOD to 820 and b LOD to 89 ng/g LW. Other nBFRs such as
tetrabromobisphenol-A (TBBPA) hexabromobenzene (HBB) and pentabromoethylbenzene (PBEB) in Asian
avifauna have been reported in very few studies. Dependence of organohalogens on dietary sources and subse-
quent biomagnification in the food chain has been corroborated through δ15N and δ13C stable isotope proxies.
In general, tissues with higher fat content accumulated more organohalogens and vice versa. Aspects such as
maternal transfer of OHCs and temporal trends have rarely been discussed in reported literature from Asia.
The mobility of birds, vicinity to sources and trans-boundary movement of pollutants were identified as key
exposure routes and subsequent OHCs contamination in Asian birds. There is extreme scarcity of literature on
organohalogen contamination in birds from Northern, South-eastern and west Asian countries where an
industrial boom has been witnessed in the past few decades. Current scenarios suggest that levels of OHCs,
particularly the FRs, are rising in birds of Asia and it would be wise to develop baseline information and to
regulate the OHCs emission accordingly.
© 2015 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412
2. Bioaccumulation of organohalogens in Asian birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
2.1. Levels of legacy POPs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
2.2. Levels of emerging flame retardants (FRs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417
3. Comparison between legacy and emerging contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
4. Regional differences in Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
5. Global scenario . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421
6. Tissue specific contamination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
7. Influence of dietary exposure and trophic levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
8. Migratory behavior and organohalogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
9. Data gaps and future research directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
10. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424

1. Introduction
The presence of organohalogens in the environment and their
adverse effects on biota is at the epicenter of modern environmental
challenges along with climate change and habitat degradation. These
pollutants are toxic organic substances that resist degradation, can
travel through long distances, bioaccumulate and biomagnify through
the food web and consequently pose a serious potential threat to
humans and wildlife (Elliott et al., 2009; Hong et al., 2014). Throughout
the developing and developed world various chemicals commonly
known as “persistent organic pollutants” (POPs) have been extensively
used in various industrial and agricultural processes until the end of the
20th century. In the later half to the last quarter of the 20th century,
flame retardants (FRs) have been introduced in the modern industry
to make the products fire resistant (Sun et al., 2014a). To combat
these perilous compounds, initially in the Stockholm convention
(2001), about a dozen of the most concerning organic contaminants
including eight different organochlorine pesticides (OCPs), two
industrially produced [polychlorinated biphenyls (PCBs) and hexachlo-
robenzene (HCB)] and two industrial byproducts [polychlorinated
dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans
(PCDFs)] have been termed as “legacy POPs” and regulated for future
use. Similarly “emerging pollutants” are referred to as different flame
retardants (FRs), surfactants, steroids, hormones, pharmaceuticals and
personal care products, among which emerging flame retardants are
of most public concern due to their increasing use in industries and ad-
verse implications on humans and animals (Li et al., 2014). So far a total
of 22 different organohalogens have been ratified as most concerning
organic compounds, out of which 18 were targeted for elimination,
two for restricted use and others for reduced unintentional release
through best available techniques/best environmental practices
(Stockholm convention 2011). Historically used legacy POPs have
attracted greater attention due to their exacerbated levels in the envi-
ronment and subsequent adverse effects on humans and wildlife (Law
et al., 2014; Wang et al., 2011). Flame retardants on the other hand
are another and relatively newer group of organic contaminants with
similar recalcitrant properties and toxic effects in the environment
and used in different industrial products such as rubber, plastics, poly-
urethane foams, and a variety of electronic and electrical appliances to
make them fire resistant (Alaee et al., 2003; Mo et al., 2012). To avoid
the future adverse effects of these compounds, efforts are underway
through various international agreements, the target of which is to reg-
ulate and curtail the global and/or regional production and usage of
these noxious chemicals (UNEP, 2011). After regulations and subse-
quent bans on the production and use of different compounds, the levels
of these historically used POPs and some legacy FRs has dropped signif-
icantly in Europe and the USA, but this decline remain unobserved in
Asian countries (El-Shahawi, 2010).
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
Asia is the biggest continent with a total terrain area of about
44,391,162 km2 and having about 60% of the global human population.
Because of increasing human population in most of the Asian countries,
agricultural activities with industrialization and urbanization have
exponentially increased during the past few decades, particularly in
East Asian regions such as China, South Korea, Japan and Russia. The
industrial activities are also on the rise in most of South Asian countries
including India, Pakistan and central to North and North-western Gulf
states, Iran and Turkey (Ali et al., 2014; Kunisue et al., 2003). This
upsurge in industrial and agricultural activities has led to either
intentional or unintentional discharges of a wide range of hazardous
chemicals in the environment including legacy POPs and emerging
FRs. Despite regulated, considerable levels of legacy POPs and FRs
have been reported in different environmental compartments such as
soil, sediments, air and water from the central, South-East and East
Asian countries indicating the illegal production/use, improper disposal
and recycling of these contaminants (Yadav et al., 2015; Ali et al., 2014;
Li et al., 2014; Hong et al., 2014; Syed et al., 2013; Wu et al., 2012; Zhang
et al., 2011b; Malik et al., 2011b; Chen and Hale 2010; Behrooz et al.,
2009). There is however, scarcity of reported studies from the Asian
continent on accumulation and toxicity of these toxic compounds in
wildlife, particularly in birds.
Over the past few decades, birds have been successfully proven as
one of the most favorite candidate group of animals to predict environ-
mental health and tracing footprints of environmental pollutants
(Gómez-Ramírez et al., 2014; Summers et al., 2010; Burger 1993,).
A few unique characteristics associated with birds such as their agility,
mobility, longevity in the ecosystem, occupying variety of habitat with
different feeding and breeding habits, possession of irreplaceable tissues
like eggs, feathers and preen glands/oil etc. make them unique creatures
from which important information about environmental quality and
pollutants prevalence can be assessed (García-Fernández and Espín,
2013; Jaspers et al., 2013). Like many other groups of contaminants,
POPs including emerging FRs have also been measured in avian tissues
to get an overview about the levels, behavior, biomagnification,
fate and implications of these noxious compounds in the biosphere
(Gómez-Ramírez et al., 2014; Chen and Hale 2010). In birds, these
compounds cause various behavioral, neurological and physiological
abnormalities that affect the reproduction and health of species and
ultimately affect the population dynamics (Connell et al., 2003;
Kunisue et al., 2006). It is customary to monitor the concentrations of
these compounds in different avian tissues and investigating their
toxicological implication upon individuals and population dynamics
(Smits and Fernie 2013; Bourgeon et al., 2012). Birds reflect the envi-
ronmental concentrations of organohalogens in a region which largely
depends upon the age, gender, feeding and movement of the birds
(Eulaers et al., 2014b; Luo et al., 2009b). Beside these functions, varia-
tions in the levels of organohalogens have been recorded among various
tissues, trophic levels, taxonomic groups and also at a spatial and tem-
poral scale (Behrooz et al., 2009; Kubota et al., 2012). Predatory bird
species have been found to be most effective indicator species, because
of their top position in the ecosystem and comprising of valuable infor-
mation about the levels of POPs, flame retardants and other contami-
nants throughout the food chain (Chen et al., 2009). Since the toxicity
concerns of conventional POPs and emerging FRs in the birds has
come into the spotlight, a huge stack of literature has been reported
from different regions of the world during the last two decades dealing
with the levels, behavior, distribution and effect of these toxic organic
compounds in various bird species. In Europe and USA a lot of literature
upon this issue is available and still progressing (Gómez-Ramírez et al.,
2014; Yordy et al., 2013; Chen et al., 2010), but huge data gaps exist in
other continents like South America, Africa, and Asia (Chen and Hale,
2010). Asia being the biggest continent and rendering a home for a
huge portion of global avifauna, has a dearth of literature reporting
the levels and toxicity of legacy POPs and emerging FRs in birds. To
summarize the reported studies on organohalogens contaminants
413
in birds, we reviewed the whole of published research articles on
this topic from different parts of the Asian continent reporting the
levels of various legacy POPs and emerging FRs in various tissues of
different bird species. Furthermore, we discussed the pattern of
organohalogen accumulation in birds based on differences in dietary
sources, migratory habits and exposure of bird species. We used
Google Scholar, SpringerLink, ISI Web of Science, PubMed and
ScienceDirect as web sources to obtain the published literature. We
used different combinations of contaminant names and Asian countries
as keywords along with Asia, birds, passerine, predators, contamination,
and species and/or tissues names etc. Finally, we tried to identify
and highlights the data gaps in reported literature from Asia on
bioaccumulations and toxicity in birds and suggest some future
research directions to resolve these issues. In the text we have pre-
sented the concentrations as round off means (ranges) derived
from the reported literature in ng/g lipid weight (LW; after conver-
sion where necessary) unless mentioned otherwise, whereas the
details have been provided in respective tables (Supplementary
information, 1 & 2).
2. Bioaccumulation of organohalogens in Asian birds
The Asian continent extends from the Northern permafrost
regions of Russia to the Southern Indo Malayan region, and from
the far Eastern industrial states such as China, Japan and Korea to
the developing South Asian region and Gulf countries, Middle East
states up to Turkey westwards. Due to huge climatic and geographi-
cal variation, this region supports a large number of bird species. A
variety of bird species ranging from sea birds, shore birds, water
birds up to the passerines and terrestrial birds are inhabitants of
the Asian continent. Besides these, Asia has a very unique avifauna
of scavengers including critically endangered vultures, birds of prey
and waterbirds. Birds in this region mostly get contaminated by the
organic pollutants that are either locally discharged or through
trans-boundary movement of these pollutants (Hong et al., 2014).
Migratory birds visit certain polluted areas and get contaminated at
their stopover sites (Kunisue et al., 2002). Asia has three of the
world important flyways namely East Asian/Australian flyway
(EAA) central Asian (CA) flyway and West Pacific (WP) flyway with
a large number of migratory species (Huang et al., 2013). In this
region, legacy POPs mainly originate from agricultural and industrial
sources, disposal sites, industrial or domestic waste and e-waste
recycling facilities (Malik et al., 2011a; Sarkar et al., 2008; Li et al.,
2014). FRs are majorly introduced in the Asian environment from
domestic and industrial wastes, leaching of products and e-waste
recycling sites (Sepúlveda et al., 2010). Levels of organohalogens
vary in different parts of Asia depending upon the extent of
agricultural, industrial and e-waste recycling activities along with
the species specific factors like type of species and/or tissues,
feeding, exposure and migratory behavior. In Asia, different species
particularly passerines, waterbirds, seabirds and predatory birds
from a variety of feeding guilds and migratory behaviors have been
studied for organohalogen contamination. Moreover levels of
organohalogens have been recorded in tissues such as eggs, liver,
kidney, blood, muscle, feathers, preen oil and whole homogenized
body. We split the further discussion on organohalogens in Asian
birds into legacy POPs and emerging FRs.
2.1. Levels of legacy POPs
Legacy POPs such as PCBs, dichlorodiphenyltrichloroethane (DDTs),
hexachlorocyclohexanes (HCHs), hexachlorobenzene (HCB), cyclodienes
(aldrin, dieldrin, endrin, etc., chlordanes (CHLs), dioxin related
compounds (DRCs) including PCDD/Fs and dioxin like coplanar
PCBs (co-PCBs) have been reported in different studies from differ-
ent parts of Asia. In Asia, legacy contaminants often make their way
414 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426

to the environment through release from various industrial and agri-
cultural sources. Compounds such as PCBs are used as a coolant in
electric and electronic equipment like transformers and capacitors.
Although the use of PCBs has been limited in Asia since past few de-
cades but there are reports that these compounds are still used in
many of the Asian countries. In the Asian environment, PCBs are
often released in the environment because of leakages of the landfills
and through leaching. Higher concentrations of PCBs in the industri-
alized countries are evidently associated with their robust industrial
setups. On the other hand, compounds such as DDT, HCHs, HCBs,
toxaphene, chlordane, aldrin and mirex are the commonly used
pesticides in the most of the Asian countries. In Asia, these groups
of pesticides and non-pesticides chemicals are released through
industrial and/or agricultural sources and then transported in the
environment through various atmospheric processes. Once reached
in the environment these compounds bioaccumulate in biotic tis-
sues, biomagnify in the food chain and subsequently poses various
risks. Table S.I. 1 summarizes the derived mean concentrations and
ranges of different legacy POPs reported in different studies from
the Asian continent. Reported concentrations of POPs in different
species, locations, feeding groups, tissues and migratory habits
have been listed under each category from the reported literature.
Depending upon the derived mean concentrations reported in Asian
birds since last two decades, legacy POPs followed the trends as
PCBs N DDTs N PCDF N PCDDs N HCHs N chlordane N cyclodienes N HCB.
PCBs mean concentrations exhibited large variations from different
regions of Asia. Mean levels of PCBs and DDTs (the most frequently
reported legacy compounds) throughout Asian continent have been
presented on a map (Fig. 1).
PCBs in Asian birds have been reported as low as below limit of
detection (bLOD) to as high as 14,000,000 ng/g LW. Maximum means
(ng/g LW) of PCBs of 282,775 (1400–7,700,000) were reported in
multiple species from Ehime University, Japan (Kunisue et al., 2008)
followed by 160,190 (600–240,000) in different resident birds of
Japan (Kunisue et al., 2003), 32,160 (960–14,000,000) in waterbirds of
an e-waste recycling region from South China (Luo et al., 2009b),
29,933 (7770–53,300) in ivory gull (Pagophila eburnea) from Arctic
region of Russia (Miljeteig et al., 2009) and 19,543 (14–674,000) in
different birds species from South Korea (Hong et al., 2014), whereas
the lowest recorded mean levels were 1.63 ng/g LW in multiple species
of birds from Japan (Kunisue and Tanabe 2009) and 3.82 (0.01–29.7)
ng/g LW in predatory birds from North China (Chen et al., 2009).
Relatively higher levels of mean PCBs at 4624 (20–140,000) in multiple
species from lake Baikal, Russia and 3885 (3.50–170,000) ng/g LW were
reported from South India (Kunisue et al., 2003). Similarly, an elevated
mean PCBs level at 3876 (159–27,000) ng/g LW has been recorded in
different waterbirds from South Korea (Choi et al., 2001a). Choi et al.
(2001b) recorded relatively greater PCBs levels of 3611 (1310–6892)
in black tailed gull (Larus crassirostris) from Hokkaido, Japan while it
was 2450 (100–36,000) ng/g LW in common kingfisher (Alcedo atthis)
from Lake Biwa, Japan (Kubota et al., 2004). Likewise, higher PCBs con-
centrations at 2618 (191–11,100) in piscivorous birds of South Korea
(Wang et al., 2011), 2061 (823–4150) in water birds of South China
(Lam et al., 2008) and 1800 (490–300) ng/g LW have been documented
in common kingfisher from South China (Mo et al., 2013b). Moderate
values for PCBs were reported from different regions of the Asian
stretch, such as 1603 (3.0–21,545) in water birds of Turkey (Kocagöz
et al., 2014), 1416 (140–73,000) ng/g LW in light vented bulbul

Fig. 1. Comparative mean concentrations (ng/g LW) of PCBs and DDTs in birds from different regions of Asia. Data from Peng et al., 2015a (A), Hong et al., 2014 (B), Kocagöz et al., 2014 (C),
Sun et al., 2014a (D), Yu et al., 2014 (E), Ito et al., 2013 (F), Mo et al., 2013a(G), Yu et al., 2013 (H), Rajaei et al., 2011 (I), Wang et al., 2011 (J), Zhang et al., 2011a (K), Behrooz et al., 2009 (L),
Chen et al., 2009 (M), Gao et al., 2009 (N), Lam et al., 2008 (O), Sanpera et al., 2003 (P&Q), Kunisue et al., 2002 (R), Choi et al., 2001a (S), Choi et al., 2001b (T), Luo et al., 2009b (U), Kunisue
et al., 2008 (V) and Kunisue et al., 2003 (W).
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
(Pycnonotus sinensis) from South China (Sun et al., 2014a) and 1435
(0.3–8385) ng/g dry weight (DW) in little egret (Egretta garzetta)
from Pakistan (Sanpera et al., 2003). Connell et al. (2003) reported
mean concentrations of 960 (270–1700) and 230 (85–600) ng/g LW
in little egret and black-crowned night heron (Nycticorax nyticorax)
from Hong Kong South China. Sun et al. (2014a) found that penta-,
hexa-, hepta- and octa-PCBs were most prevalent constituting more
than 90% of total PCBs. Further they concluded that PCBs in birds from
South China mainly derived from e-waste disposal and recycling sites.
Relatively lower mean levels (ng/g LW) at 809 (290–2547) in streaked
shearwater (Calonectris leucomelas) from different Islands of Japan (Ito
et al., 2013), 608 (48–14,000), 694 (63–3600) in multiple birds species
of Philippines and Vietnam (Kunisue et al., 2003) and 576 (23–71,000)
in multiple birds species from North China (Yu et al., 2013) have been
documented. Similarly, lower mean PCBs concentrations on a wet
weight (WW) basis of 494 (0.9–52,000) in different water bird species
from South China (Zhang et al., 2011a), 236 (b20–44,000) in multiple
species from South India (Tanabe et al., 1998), 226 (b LOD-4089), in dif-
ferent waterbirds from Caspian sea coast of Iran (Rajaei et al., 2011), 168
(6.5–4400) in multiple species of South India (Senthilkumar and
Kannan, 2001b) and 23 (7–30.5) ng/g (WW) have been detected in
multiple species of Velar River, South India (Ramesh et al., 1992). In con-
trast, Liu et al. (2010) reported a relatively moderate concentration at
283 (38–1700) ng/g LW in multiple bird species from South China.
Peng et al. (2015a) reported a mean ortho-substituted PCBs concen-
trations of 200 (45–1770) ng/g LW, dominated by PCBs with 5 to 7
chlorines in passerine birds from South China. Similarly, Yu et al
(2014) reported the mean concentrations at 88 (26–540), 59 (23–720)
and 87 (25–500) in passerine birds from three metropolitan cities of
China; Guangzhou, Beijing and Wuhan respectively. Gao et al. 2009
found a mean level at 181 (0.4–1006) ng/g LW of PCBs in different bird's
species from China whereas somewhat lower level were reported at
150 ng/g LW in thick billed reed warbler (Acrocephalus aedon) from cen-
tral China (Nakata et al., 2005), and 22 (b LOD-82) ng/g LW in different
birds from Iran (Behrooz et al., 2009). This indicates that the regions
with lower PCBs concentrations may utilize less conventional PCBs
and/or it may be due to scarcity of reported information from these
locations. Overall reported data indicates that PCBs are much more
prevalent in China, Japan, South Korea and Russia respectively
(Fig. 1).
DDTs concentrations in Asian Aves vary from as low as bLOD to as
high as 790,000 ng/g LW. The highest mean concentration (ng/g LW)
of DDTs of 54,500 (9600–310,000) ng/g LW was recorded in greater
cormorant from Sagami River Japan (Kumar et al., 2005) followed by
mean levels (ng/g LW) at 35,159 (40–45,500) in multiple bird's species
from South Korea (Hong et al., 2014) and 30,756 (7870–48,650) in dif-
ferent species of water birds of South China (Lam et al., 2008). Bottom
concentrations of DDTs were reported at 69.06 (not detected (nd) to
372) in cattle egret from Pakistan (Malik et al., 2011a), 39 (0.1–1024)
in predatory birds of North China (Chen et al., 2009), 24 (1.0–295) in
multiple bird species of Khuzestan, Iran (Behrooz et al., 2009) and the
lowest documented mean of 19 (1.6–370) in water birds from South
China (Zhang et al., 2011b). A general trend of DDTs mean concentra-
tions (ng/g LW) reported in different resident and migratory birds
species from Asian countries were as; Japan 23,429 (600–240,000),
South India 8054 (3.4–170,000), Vietnam 6782 (390–77,000),
Philippines 2903 (48–14,000) and Russia 2562 (20–140,000) respec-
tively (Kunisue et al., 2003). A relatively higher mean level of DDTs at
3415 (89–150,000) has been documented in a mix of bird species
from Northern China (Yu et al., 2013). Further, elevated mean DDTs
concentrations (ng/g LW) at 9581 (186–68,000) in ivory gull from
Russian Arctic region (Miljeteig et al., 2009), 7292 (400–49,000) in
waterbirds from Hong Kong (Wang et al., 2011), 5100 in thick-
billed reed warbler from Shanghai, China (Nakata et al., 2005),
3854 (2.1–15,640) in multiple birds species from Yellow River
delta, North China (Gao et al., 2009), 2432 (9.2–26,000) in different
415
waterbirds from Lake Baikal region, Russia (Kunisue et al., 2002),
2112 (272–21,192 DW) in little egret from Pakistan (Sanpera et al.,
2003), 1907 (33–8680) in waterbirds of Nakdong River of South
Korea (Choi et al., 2001a), 1714 (828–3578) in black tailed gull
from Hokkaido, Japan (Choi et al., 2001b) and 1267 in streaked
shearwater have been reported from different islands of Japan
(Ito et al., 2013). An elevated mean DDTs concentration of 2400
(550–6400) ng/g LW has been documented in common kingfisher
from South China (Mo et al., 2013b). The average of all the median
concentration of DDTs reported in different tissues of water birds
from Turkey was around 1849 (1.0–17,625) ng/g LW (Kocagöz et al.,
2014). Connell et al. (2003) reported the mean DDTs levels (ng/g LW)
of 1200 (560–2200) and 600 (210–1200) in little egret and black-
crowned night heron from South China, respectively. In passerine
birds from different parts of China, DDTs median concentrations
(ng/g LW) were 493 (38–5270) from South China (Peng et al.,
2015a), 150 (23–880) from Guangzhou, 340 (89–11,000) from
Beijing and 1500 (690–19,000) from Wuhan (Yu et al., 2014). Luo
et al. (2009b) reported a moderate mean DDTs concentration
of 882 (51–6900) ng/g LW from an e-waste recycling region
from South China. Relatively lower mean DDTs concentrations of 733
(1.3–13,000) and 471 (0.3–13,000) ng/g WW were documented in
multiple species from Tamil Nadu, India (Senthilkumar and Kannan,
2001b; Tanabe et al., 1998) followed by 562 (4.4–13,077) ng/g DW in
cattle egret from Pakistan (Khan et al., 2013), 392 (bLOD to 9040) ng/g
WW in waterbirds from Caspian sea coast, Iran (Rajaei et al., 2011) and
129 (12 to 4600) ng/g LW, in light vented bulbul (P. sinensis) from
South China (Sun et al., 2014a). Similarly, Ramesh et al. (1992) reported
a relatively lower mean level of 171 (1.9–430) ng/g WW of DDTs in dif-
ferent birds from Vellar River, South India. In different studies on DDTs
levels in Asian birds, p,p′ DDE (dichlorodiphenyldichloroethylene) was
unanimously documented as the most prevalent metabolite contributing
more than 90% (in most cases) of DDTs (Peng et al., 2015a; Yu et al.,
2014; Sun et al., 2014a; Wang et al., 2011). DDTs have long been used
in Asian agriculture and remains are still found in the environment and
biotic tissues. It is thought that even after the ban in almost all the
Asian countries DDTs have still been used illegally in different parts of
Asia (Zhang et al., 2011a). Like PCBs, concentrations of DDTs were com-
paratively higher in Japan, China, South Korea and India, whereas infor-
mation on DDTs is also absent in many important parts of Asia (Fig.1).
HCHs concentrations in Asian birds range from b LOD to 29,000 ng/g
LW. The lowest mean HCHs concentration of 3.07 (0.08–37.5) ng/g LW
has been recorded in different birds of prey from North China (Chen
et al., 2009) while the maximum mean level of 7352.3 (180–29,000)
has been detected in multiple birds species of South India (Kunisue
et al., 2003). Elevated mean of HCHs was recorded in multiple birds
from Vietnam 237 (6.4 to 2800) followed by, Philippines 298 (1.0 to
3700), Russia 430(3.0 to 9000) and Japan 1443(17 to 13,000) ng/g LW
respectively (Kunisue et al., 2003). Comparatively high mean concen-
trations (ng/g LW) of HCHs such as 1119 (117–2084) ng/g DW (Khan
et al., 2013), 232 (nd-178.9) (Malik et al., 2011a) and 100 (44.7–858)
(Sanpera et al., 2003) have been documented in waterbirds from
Pakistan. Similar levels of HCHs accumulation on wet weight basis
such as 990 (14–5500) (Tanabe et al., 1998), 928 (21–7000)
(Senthilkumar and Kannan, 2001b) and 375 (23–1040) ng/g WW
(Ramesh et al., 1992) have been reported in multiple birds from
South India. Luo et al. (2009b)documented a mean level of HCHs as
562 (39–4200) in waterbirds species collected from an e-waste region
of Pearl River delta, South China. Similarly elevated mean HCHs levels
of 708, 485 and 426 with corresponding ranges of 23 to 3220; 120 to
1800 and 3 to 9000 ng/g LW have been measured in multiple species
of Korea (Hong et al., 2014), greater cormorant of Sagami River Japan
(Kumar et al., 2005) and water birds of Lake Baikal Russia (Kunisue
et al., 2002) respectively. Relatively moderate levels (ng/g LW) of
mean HCHs accumulations of 250 in thick-billed reed warbler from
Shanghai (Nakata et al., 2005), 239 in multiple birds of North China
416 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
(Gao et al., 2009), 183 in water birds from South Korea (Choi et al.,
2001a) 170 in black tailed gull from Japan (Choi et al., 2001b) and
135 have been reported in water birds from Turkey (Kocagöz et al.,
2014). In contrast, lower mean concentrations of 39 (20–87.9) and
12 (0.9–99) ng/g LW of HCHs have been reported in streaked shear-
water from Japan (Ito et al., 2013) and different terrestrial birds from
South China (Zhang et al., 2011a). Similarly, lower HCHs mean concen-
trations of 37 in multiple species (Behrooz et al., 2009) and 21 ng/g LW
in water birds (Rajaei et al., 2011) were documented from Iran. Very
low corresponding HCHs concentrations (ng/g LW) in little egret
17 (12.2–21) and black-crowned night heron 21 (8.3–30) have been
documented from South China (Connell et al., 2003). HCHs are
pesticides which have been used for long time in Asian continent but
the available data on HCHs contamination in birds is very little.
Dioxin like or coplanar PCBs in Asian avifauna oscillated between
minimum as bLOD to maximum 150,000 ng/g LW. Highest mean con-
centration of co-PCBs being 31,500 (4500–150,000) in common cormo-
rant has been documented from Sagami River Japan (Kumar et al., 2005)
whereas the lowest mean concentration of 7 (2.5–12.7) ng/g LW have
been recorded in black tailed gull (L. crassirostris) from Japan (Kubota
et al., 2006). A very high mean concentration of 10,125 ng/g LW for
co-PCBs has been measured in multiple species from Tokyo Japan,
where the omnivorous species accumulated the highest co-PCBs
mean (ng/g LW) of 29,266 followed by carnivorous 8842, piscivorous
2343 and grainivorous 50, respectively (Senthilkumar et al., 2002).
Similar mean concentrations of co-PCBs of 2430 (695–6530) and 2450
(100–3600) ng/g LW have been reported in Ivory gull from Russia
(Miljeteig et al., 2009) and common cormorant from Lake Biwa, Japan
(Nakata et al., 2005) respectively. Wang et al. (2012) reported a mean
359 (2.56–962) ng/g LW of mono-ortho PCBs with PCB-118 the most
prevalent congener constituting more than 98% of the total co-PCBs.
A moderate mean concentration of 150 (23–1770) ng/g LW has
been detected in black eared kite (Milvus migrans) from district
Kanto, Japan. Relatively lower mean concentrations of co-PCBs as
58 (0.19–169.57) and 44 (31.76–55.83) ng/g LW have been reported
in seabirds of Torishima island, Japan (Kunisue et al., 2006) and
predatory birds of Coimbatore, South India (Senthilkumar et al.,
2001a). Kubota et al. (2012) detected lowest mean concentration
on wet weight basis of 4.4 (ng/g WW) in liver of common cormorant
from Lake Biwa Japan. In general, all dioxin like PCBs were reported
in lower concentrations and also in less number of studies in Asian
birds than total PCBs and other OCs.
PCDD/Fs contamination in Asian birds has only been investigated
in very small number of studies, mostly from Japan. The ranges of
concentrations of PCDDs, PCDFs and PCDD/Fs reported in Asian
birds were b LOD to 27.45; bLOD to 45.90 and 0.02 to 73.73 ng/g LW
respectively, with maximum level recorded in carnivorous species.
The concentrations of PCDDs, PCDFs and PCDD/Fs at 3.31, 1.27,
4.70 for piscivorous; 2.30, 3.02, 5.33 for omnivorous and 0.24, 0.16,
0.40 ng/g LW for grainivorous species have been reported from
Tokyo Japan (Senthilkumar et al., 2002). Mean concentrations of
PCDDs and PCDFs as 0.23 (0.03–0.53) and 0.57 (0.09–0.93) ng/g
LW were recorded in different tissues of sea birds from Torishima
Island, Japan (Kunisue et al., 2006). Lowest mean concentrations for
PCDDs, PCDFs and PCDD/Fs at 0.02 (0.00–0.08), 0.02 (0.01–0.03) and
0.05 (0.02–0.12) have been recorded in black tailed gulls from
Hokkaido, Japan respectively (Choi et al., 2001b). In comparison,
mean concentrations of 2.51 (0.03–2.9); 0.48 (b0.4–1.7) and
8 (1.7–27) ng/g LW have been reported in fish eating common
cormorant from Sagami River Japan (Kumar et al., 2005). Similarly,
mean concentrations of 1.5 and 2.5 ng/g WW have been recorded
in a temporal (2001–2008) variation investigation on common cor-
morant in Lake Biwa Japan (Kubota et al., 2012). Senthilkumar
et al. (2001a)reported a moderate mean concentrations of PCDDs
of 0.98 (b0.1–2.7), PCDFs of 0.48 (b0.1–1) and PCDD/Fs of 1.43
(0.04–3.3) in carnivorous birds of South India respectively. Similarly
Kunisue et al. (2003)reported mean levels of 1.14 (0.39–1.70) for
PCDDs, 1.01 (0.06–1.5) for PCDFs and 1.85 (0.18–2.9) ng/g LW in
common cormorant from Lake Biwa Japan (Kubota et al., 2004).
Very low mean concentrations of PCDDs, PCDFs and PCDD/Fs of
0.09 (nd-1.05), 0.1 (0.01–0.06) and 0.2 (0.02–1.3); 0.6 (0.1–4.1),
0.1 (0.03–0.9) and 0.7 (0.1–4.2) ng/g LW have been recorded in
water birds from Nakdong River, South Korea (Choi et al., 2001a)
and Hong Kong (Wang et al., 2012), respectively. In general, levels
of PCDD/Fs were higher in fish eating water birds and carnivorous
species but like many other contaminants they are less documented
in Asian birds.
CHLs, which include different compounds such as heptachlor,
oxychlordane, nonachlor, etc., have been documented at a limited
scale in Asian birds. We have emphasized to compare total chlordane
concentrations because of scarcity of reported literature on different
individual compounds specifically. CHLs concentrations recorded in
Asian bird species were as low as bLOD to as high as 47,000 ng/g LW.
The mean concentrations of CHLs was highest as 4450 (700–16,000)
ng/g LW in great cormorant from Sagami River, Japan (Kumar et al.,
2005). Lam et al. (2008) reported mean levels of heptachlor and total
chlordane of 37 and 985 ng/g LW in waterbirds collected from three
different cities of China. In the same study, the total chlordane levels
were 1760, 914 and 279 from Hong Kong, Xiamen and Quanzhou
cities respectively. Relatively elevated mean concentrations at 843.6
(9.95–3160) and 392.35 (b 0.1–6030) ng/g LW, have been reported in
waterbirds of Hong Kong (Wang et al., 2011) and in different coastal
bird species of South Korea (Hong et al., 2014). In multiple birds species
collected from different countries of the Asian stretch, the means of
total chlordanes (ng/g LW) reported were 27.56 (b0.1–600) in
India; 55 (4.1–150) in the Philippines; 72 (1.8–200) in Vietnam;
80 (1.2–1300) in Lake Baikal (Russia) and 3946 (59–47,000) from
Japan respectively (Kunisue et al., 2003). Similarly, Kocagöz et al.
(2014) reported a mean chlordane level of 100 (nd-712) ng/g LW
in different tissues of water birds from Turkey. In waterbirds from
Hong Kong a mean concentration of 44 and 844 ng/g LW has been
reported for heptachlor and total chlordane (Wang et al., 2011).
In another study conducted in Hong Kong, mean concentrations
(ng/g LW) of ∑ chlordane of 280 (81–470) and 31 (59–75) have
been documented in little egret and black crowned night heron,
respectively (Connell et al., 2003). Similarly, in predatory birds a
mean heptachlor epoxide level of 49 (nd-918) ng/g LW has been
recorded from North China (Chen et al., 2009). Moderate concentra-
tions of 128.8 and 87.5 ng/g LW for ∑ chlordane have been reported
in waterbirds from South Korea (Choi et al., 2001a) and black
tailed gull from Japan (Choi et al., 2001b). A mean value of 20 ng/g
LW for ∑ chlordane was recorded with a highest contribution of
oxychlordane in the thick billed reed warbler from Shanghai, China
(Nakata et al., 2005). Total chlordane mean concentrations of
59 ng/g DW (Khan et al., 2013) and 12.3 ng/g LW (Malik et al.,
2011a) have been recorded in waterbirds of Pakistan. Chlordane
mean concentrations (ng/g WW) with lowest values of 1.2 (nd-24)
(Senthilkumar and Kannan, 2001b) and 2.12 (0.1–45) (Tanabe
et al., 1998) have been reported in multiple birds species from
Tamil Nadu region, South India. Although mostly reported in lesser
concentrations, information on chlordane is scarce in Asian birds.
HCB levels have been recorded in Asian birds as low as b LOD to
as high as 12,000 ng/g LW. Maximum mean HCB concentration
of 835 (180–2800) ng/g LW in common cormorant from Sagami
River Japan (Kumar et al., 2005) and lowest mean level 0.245
(0.07–0.59) ng/g WW was found in multiple bird's species from
Vellar River, South India (Ramesh et al., 1992) respectively. Elevated
mean concentrations ng/g LW of HCB of 747 (396–110) in ivory gull
from Russian Arctic area (Miljeteig et al., 2009), 685 (1.5–5900) in
different species of South Korean birds (Hong et al., 2014) and 112
(8.03–1940) in water birds from Hong Kong (Wang et al., 2011) have
been recorded. Kunisue et al. (2003) reported mean HCB concentrations
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
(ng/g LW) of 665 (10–12,000) in multiple birds of Japan followed by 37
(1.0–250) in Vietnam, 17 (b0.1–350) in India and 15 (0.1–920) in
Philippines. In the coast of South China Sea mean HCB concentrations
of 290, 149 and 70 ng/g LW were reported in waterbirds from
Quanzhou, Hong Kong and Xiamen port cities respectively (Lam et al.,
2008). Mean concentrations of HCBs were 89 (53–190) ng/g LW in
black tailed gull from Japan (Choi et al., 2001b) and 88 (8–332) ng/g
LW in different species of waterbirds from Nakdong River, South
Korea (Choi et al., 2001a). Comparatively lower mean HCB values as
32 and 18 ng/g LW have been reported in thick billed reed warbler
from Shanghai (Nakata et al., 2005) and different birds species from
Khuzestan province, Iran (Behrooz et al., 2009) respectively. Similarly
the mean concentrations for HCBs (ng/g WW) were 62 (b LOD to
1271), 1.43 (b0.1 to 23) and 0.90 (b LOD to 7.8) in waterbirds from
Caspian Sea coast of Iran (Rajaei et al., 2011), multiple species of
Tamil Nadu (Tanabe et al., 1998 and Senthilkumar and Kannan
(2001b)respectively. Sanpera et al. (2003) reported a mean HCBs level
of 9.43 (1.0–31.4) ng/g DW in eggs of little egret from Pakistan. HCB is
also one of the legacy POPs, which has been reported in very few studies
from Asia.
Cyclodienes such as aldrin, dieldrin and endrin etc. have been
reported in few studies as well. For the reason of scarcity of reported
information on different individual compounds, we have often taken
the cyclodienes group as a whole and compare collective concentra-
tions. Levels of cyclodienes in Asian avifauna varied from b LOD to
4600 ng/g LW. The highest mean concentration of total cyclodienes of
1090 (b 0.1 to 4600) ng/g LW has been detected in different tissues
of greater cormorant from Sagami River, Japan (Kumar et al., 2005).
A range of not detected (nd) to 8.7 of aldrin has been reported in cattle
egret from Pakistan, which is the lowest level of any cyclodiene reported
in the Asian region (Malik et al., 2011a). A total cyclodienes mean of
141.86 (0.7–886) has been recorded in different waterbirds collected
from Turkey (Kocagöz et al., 2014). Khan et al. (2013) analyzed various
OCPs in cattle egret (Bubulcus ibis) from two big cities of Pakistan and
reported mean (ng/g DW) concentrations 14, 11, 20 for total Aldrin,
dieldrin and endrin respectively, while the total cyclodienes level of
45 has been derived from this study. Similarly mean concentrations of
5.09, 69.39 and 26.46 have been reported for aldrin, dieldrin and endrin
in waterbirds from Hong Kong whereas the total cyclodienes level re-
ported in this study was around 100.94 ng/g LW, respectively (Wang
et al., 2011). A high mean concentration of 435.66 (173–1640) ng/g
LW for dieldrin has been recorded in ivory gull from the Arctic Circle
of Russia (Miljeteig et al., 2009). From three port cities of South China
namely Hong Kong, Xiamen and Quanzhou, a mean concentration of
0.20, 49.43 and 24.43 ng/g LW was recorded in water birds for aldrin,
dieldrin and endrin, whereas the total cyclodiene levels in this study
were 191, 102 and 63 ng/g LW, respectively (Lam et al., 2008). Total
cyclodienes level reported in little egret from Taunsa barrage and
Karachi harbor sites of Pakistan were 129 and 160 ng/g LW respectively
(Sanpera et al., 2003).
Mirex and toxaphene levels in birds of Asia have been documented in
a minimal number of studies. The mean values of mirex and toxaphene
of 169 (6.54–905) and 286 (2.36–1080) have been detected in water-
bird species from Hong Kong (Wang et al., 2011). Miljeteig et al.
(2009) reported an elevated level of 349 (125–713) of Mirex in eggs
of sea bird colonies from Russia. Similarly, from three different port
cities of South China, mean concentrations of 167 and 38 for mirex
and toxaphene have been recorded in eggs of different waterbird
species, respectively (Lam et al., 2008).
2.2. Levels of emerging flame retardants (FRs)
Emerging flame retardants in birds of Asian countries have been
reported in lower numbers of published studies as compared to legacy
POPs. Emerging FRs such as polybrominated diphenyl ethers (PBDEs),
decabromodiphenyl ethane (DBDPE), 1,2-bis(2,4,6-
417
tribromophenoxy)ethane (BTBPE), Hexabromocyclododecane
(HBCDs) and Dechlorane plus (DPs) have been the main focus,
while compounds like pentabromoethylbenzene (PBEB),
hexabromobenzene (HBB), Tetrabromobisphenol-A (TBBPA) and
pentabromotoluene (PBT) have been discussed at a very limited
scale in Asian avifauna. Flame retardants are relatively newer contami-
nants in the environments and they are mostly used at a large scale in
the industry to make the products fire resistant. PBDEs are the most
commonly reported flame retardant in birds from the Asian continent.
In Asia, they are commonly released through volatilization of the treat-
ed products, emissions during manufacturing, during treatments of
waste and recycling of the FRs containing products. Other flame retar-
dants such as HBCDs, DPs etc. are used as additives of brominated or
chlorinated flame retardants and mostly used in coating of electric
wires, cables, lubricants, roofing materials, furniture, textile, cushions,
packaging and electric material. In Asia, these compounds are released
from the industrial, domestic and waste dump sources, reaches in the
environment and causes various damages. Table S.I. 2 summarizes the
derived mean concentrations and ranges of different emerging FRs in-
cluding novel BFRs reported in Asian birds. It is evident from the report-
ed literature that PBDEs are the major compounds prevailing in Asian
birds, followed by HBCDs, DPs, DBDPE and BTBPE in descending order
of their mean concentrations, respectively. Like POPs, these compounds
were also measured in a variety of Asian birds including passerine spe-
cies, waterbirds, seabirds and predators etc. belonging to different tax-
onomic, trophic and migratory/resident groups of birds. Moreover the
concentrations of FRs were documented in different invasive (muscle,
kidney, liver) as well as non-invasive (blood, preen oil, feathers and
eggs) tissues. Depending upon the diet, habitat, exposure, tissues and
migratory behaviors, differential levels of emerging FRs have been re-
ported in birds of Asia. Since PBDEs are the most frequently document-
ed FRs in Asian birds their concentrations have been shown on map
(Fig. 2).
PBDEs have been reported as dominant FRs in Asian birds with BDE
47, 99, 153 and 209 as the most frequently occurring congeners,
which is linked to the exposure variation and feeding guild of the
species (Kunisue et al., 2008; Peng et al., 2015a). Concentrations of
PBDEs in Asian birds have been reported as low as b LOD to a very
high maximum of 134,000 ng/g LW. In Asian birds a minimum level of
mean PBDEs concentration of 0.92 (nd-1.49) ng/g LW has been reported
in some waterbirds species from Punjab, Pakistan (Malik et al., 2011b),
whereas the highest mean concentration of 8760 (2030–26,400) ng/g
LW has been detected in common kingfisher (A. atthis) from an
e-waste recycling facility of South China (Mo et al., 2012). A collective
PBDEs mean of about 3000 ng/g LW [individual means (ng/g LW) of
8775 (230–33,000) for inland birds, of 350 (220–530) for coastal birds
and 47 (3.3–210) for seabirds from] has been recorded in Ehime
University samples, Japan (Kunisue et al., 2008). They reported a
very high level of mean PBDEs concentrations (ng/g LW) in individual
bird species of 33,000 for goshawk (Accipiter gentilis) followed by
11,000 for Steller's eagle (Haliaeetus pelagicus), 1300 for common
crow (Corvus macrorhynchos) and 530 common cormorant. Similarly,
a very high mean PBDEs concentration of 2641 ng/g LW, with a very
high individual bird concentration (up to 40,900 ng/g LW) in Kestrel
(Falco tinnunculus) has been documented from Beijing, North China
(Chen et al. 2007) reported a mean PBDEs level of in different predatory
birds,. In comparison, the mean concentration (ng/g LW) of PBDEs were
found at 1436 (6–16,000) in waterbirds collected from an e-waste
recycling site of South China (Zhang et al., 2011b), 1409 (330–3300)
in common cormorants from Sagami river Japan (Watanabe et al.,
2004) and 1338 (61–134,000) in multiple birds species of South Korea
(Hong et al., 2014). Further elevated mean (ng/g LW) PBDEs of
93 (2.31–7483) in water cock (Gallicrex cinerea) (Shi et al., 2009),
799 (23–14,000) in different species of waterbirds (Luo et al., 2009b),
792 (56–5200) in passerine species (Sun et al., 2012a) and 424
(139–1040) in water birds (Wang et al., 2012) have been reported
418 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426

Fig. 2. Comparative mean concentrations (ng/g LW) of PBDEs in birds from different regions of Asia. Data from Peng et al., 2015a (A), Hong et al., 2014 (B), Kocagöz et al., 2014 (C), Yu et al.,
2014 (D), Mo et al., 2013b(E), Yu et al., 2013 (F), Huang et al., 2013 (G), Chen et al., 2007 (H), Watanabe et al., 2004(I), Lam et al., 2007 (J), Kunisue et al., 2008 (K), Gao et al., 2009 (L), Luo
et al., 2009b (M), Zhang et al., 2011b (N), Malik et al., 2011b (O), Sun et al., 2012a (P) and Mo et al., 2012 (Q).

from different sites at an e-waste recycling region of South China.
Sun et al. (2012a) deduced that in general, flame retardants followed
the trend as rural b suburban b urban b e-waste sites indicating that
e-waste recycling is the main reason explaining their elevated levels
in South China. Yu et al. (2011) reported a relatively higher mean
concentration at 400 (120–8500) ng/g LW in carnivorous species
compared to 250 (100–2600) in grainivorous species collected
from North China. The mean of PBDE concentrations (ng/g LW) at
190 (51–3700) and 250 (100–2600) have been recorded in passerine
birds from Guangzhou (South China) and Beijing (North China),
respectively, which were significantly higher than the mean of 32
(13–3200) reported from Wuhan (central China) (Yu et al., 2014).
This difference was due to higher urbanization and industrialization
in the former two metropoles of China. Relatively moderate levels of
PBDEs at 324 (Lam et al., 2008) and 285 ng/g LW (Lam et al., 2007)
have been recorded in water birds from different port cities of
South China. A mean concentration of PBDEs as 213 (25.4–564) has
been documented in ivory gull a “nearly threatened” designated
species from the Arctic region of Russia (Miljeteig et al., 2009).
Moderately higher concentrations in waterbirds from Turkey at
191 (0.9–3771) (Kocagöz et al., 2014), in terrestrial birds of South
China at 181 (53–423) (Sun et al., 2014b), at 89 (51–420) in common
kingfisher from a nature reserve of South China (Mo et al., 2013b)
and at 69 (0.64–580) ng/g LW in multiple species from South China
(Liu et al., 2010) have been documented for total PBDEs. Lower con-
centrations (ng/g LW) of total PBDEs at 64 (14–324) in multiple
species of Chongming Island, Central China (Huang et al., 2013),
57 (11–340) in passerine species of a nature reserve from South
China (Peng et al., 2015a) and 51 (1.1 to 233) in a mix of species
from yellow River delta, North China (Gao et al., 2009) have been re-
ported. On dry weight basis, a lower PBDEs level of 26 (1.5–7897) ng/g
has been recorded in domestic fowls from an e-waste recycling zone of
South China (Luo et al., 2009a). Similarly, a lower mean concentration of
PBDEs of 3.32 ng/g WW has been recorded in herring gull (Larus
argentatus) from Bohi bay, North China (Wan et al., 2008). The concen-
trations map indicates that most of the studies on PBDEs accumulation
have been reported from Japan, South Korea and China where they are
also found in high concentrations (Fig. 2).
HBCDs are the second highest accumulating FRs on the basis
of their mean concentrations in Asian avifauna after PBDEs, but
they have been documented in lower number of published studies.
HBCDs concentrations extended from as low as b LOD to as high
11,800 ng/g LW in Asian birds. The highest average concentration
of 567 (nd-11,800) ng/g LW for HBCDs has been reported in multiple
bird species from South Korea (Hong et al., 2014). A relatively higher
mean concentration of HBCDs at 340 (nd-5085) ng/g LW has been
reported in different birds from Pearl River delta, South China (He
et al., 2010). In contrast, a lower mean concentration of HBCDs at
63 (nd-1700) has been documented in different birds collected
from multiple locations of South China (Sun et al., 2012b). Yu et al.
(2014) reported relatively lower levels of mean HBCDs concentra-
tions (ng/g LW) at 51 (6.5–1100) in passerine species of Beijing;
3.4 (0.68–21) Guangzhou and 2.8 (2.7–14) Wuhan China. In predatory
birds from North China, mean HBCDs concentrations were recorded
more than double [133.3 (nd-440) ng/g LW] when compared to their
prey species [51 (6.5–1100) ng/g LW] suggesting biomagnification of
HBCDs similar to PBDEs in the food web (Yu et al., 2013). From the
Arctic region of Russia a mean HBCDs of 99 (14–272) has been recorded
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
in three different colonies of ivory gull (Miljeteig et al., 2009). Like most
of the FRs, it is difficult to infer any specific trends of HBCDs in Asian bird
because of scarcity of reported information.
DPs on average, accounted as the third highest recorded FR in Asian
birds. Usually the concentrations of total DPs are given in the literature
without the respective distribution of syn and anti-isomers, so for
comparison we have mostly used the levels of total DPs. Minimum con-
centrations at b 0.1, b 0.1, b LOD to maximum concentrations at 920,
2900 and 3820 ng/g LW have been recorded for syn, anti-isomers and
total DPs from Asian species. A maximum mean DPs level of 228
(0.60–3820) ng/g LW with syn-isomers value of 48.20 (b 0.1 to 920)
and anti-isomers of 218 (b0.1 to 2900) has been recorded in predatory
birds from Beijing, North China (Chen et al., 2013). In the same study a
positive correlation in fanti (ratio between anti isomers to total DP's con-
centrations) and ∑DPs was found in Eurasian sparrowhawk (Accipiter
nisus) tissues suggesting that DP bioaccumulation in terrestrial species
is mainly driven by the level of anti-isomers and some factors other
than lipid solubility may significantly affect the total DPs levels in
different avian tissues. Contrary to this, lowest mean concentrations of
1.52 (0.1–68.2), 4.32 (1.2–35.7) and 595 (1.2–104) ng/g LW have
been recorded for syn, anti-isomers and total DPs in passerine species
collected from a nature reserve of South China (Peng et al., 2015b).
Higher liver concentrations for syn, anti and total DPs at 60 (0.95–420),
173.5 (6.1–920) and 233.9 (7–1300) have been documented when
compared to the corresponding concentrations at 10 (0.53–280),
34 (3.4–650) and 45 (3.9–930) in the muscle tissues collected from mul-
tiple birds species of South China (Sun et al., 2012c). Zhang et al. (2011b)
recorded a high mean value of 147 (nd-2200) ng/g LW for total DPs in
water birds collected from an e-waste recycling area of South China.
Similarly, a higher mean concentration of 56 (4.6–268) ng/g LW for
total DPs has been reported in terrestrial bird species from South China
(Sun et al., 2014b). Mean concentrations of DPs were higher at 25.25
(nd-500) in predatory birds when compared to 4.9 (nd-31) ng/g LW in
prey birds species from Beijing, China (Yu et al., 2013). Furthermore,
they reported quite similar fanti values to those of commercially available
DP products indicating the similar bioaccumulation factor for syn and
anti-isomers in the terrestrial environment. In Passerine birds, median
concentrations of DPs at 13 (nd-350), 4.9 (nd-31) and 4.4 (1.7–18) ng/g
LW were recorded from three metropoles of China; Guangzhou, Beijing
and Wuhan respectively. Relatively higher concentrations of DP in South-
ern parts of China as compared to Northern parts have thought to be as-
sociated with higher e-waste recycling activities in Southern China (Yu
et al., 2014). Corresponding mean concentrations at 19 (10–50), 38
(17–99) and 58 (29–150) ng/g LW for syn, anti and ∑DPs were recorded
in kingfisher from an e-waste recycling facility which were far higher
than respective concentrations at 2 (1.2–3), 6.4 (5.4–6.5) and 3.9 (0.89–
13) ng/g LW at a reference site from South China (Mo et al., 2013a).
DBDPE levels, like other groups of FRs, have not been documented at
a great extent in Asian birds. The range of concentrations for DBDPE var-
ied between b LOD to 820 ng/g LW in Asian bird species. The highest
mean concentration at 92.5 (6.1–609) ng/g LW has been recorded in
multiple terrestrial species collected from Pearl River delta, South
China (Sun et al., 2014b). Similarly an elevated mean level of 64.2
(nd-800) of DBDPE has been detected in different waterbird species col-
lected from Pearl River delta, South China (Luo et al., 2009b). On the
other hand, the DBDPE mean concentration was found as low as 0.68
(nd-2.4) ng/g LW in a mix of bird's species from yellow river delta,
North China (Gao et al., 2009). This difference between deltas of North-
ern and Southern China has mainly been attributed to higher e-waste
recycling and industrial manufacturing near Southern sites as compared
to Northern locations. As an excellent replacement for Deca-BDE and its
high usage in electrical and electronic industries, the concentration of
DBDPE was found higher in urban locations from China as compared
to sub-urban or rural sites. Relatively higher mean concentrations of
37.17 (9.6–124) and 19.44 (3.4–37) ng/g LW of DBDPE have been
documented in water cock (Shi et al., 2009) and passerine birds (Sun
419
et al., 2012a) collected from e-waste recycling zones of South China.
Mo et al. (2013a)reported a high mean DBDPE of 23 (0.44–90) ng/g
LW in common kingfisher at Dinghushan nature reserve, South China.
Peng et al. (2015a)investigated DBDPE levels in four passerine birds of
South China and found a medians of 16 (2.7–125) ng/g LW. In a compar-
ative study of three metropoles of China Yu et al. (2014) reported me-
dians of DBDPE of 31 (2.8–390), 8.5 (nd-330) and 3.6 (0.18–820) in
passerine species from Guangzhou, Beijing and Wuhan respectively.
BTBPE concentrations have also been less documented in Asian birds.
From the published literature so far it is obvious that BTBPE is a less
prevalent FRs in bird's species from China, whereas in many parts of
Asia it has not yet been documented. However, concentrations of
BTBPE reported in other compartments and wildlife of Asian regions
suggest that it may accumulate at higher concentrations in birds feeding
because of their higher trophic position. The levels of BTBPE recorded in
birds from China (the only Asian country where BTBPE has been report-
ed) was as low as bLOD to as high as 89 ng/g LW. A maximum mean of
BTBPE at 7.7 (2.7–38) ng/g LW has been documented in common king-
fisher from an e-waste recycling facility of south China (Mo et al., 2012).
Peng et al. (2015a) reported the lowest median level of BTBPE of 0.15
(0.01–1.2) ng/g LW in passerine species collected from a nature reserve
of South China. A very low range of nd to 7.5 ng/g LW of BTBPE has been
reported in terrestrial birds from the Pearl River delta, South China (Sun
et al., 2014b). Similarly, a low relative mean value for BTBPE of 0.19
(0.04–0.87) ng/g LW has been detected in common kingfisher from
Dinghushan nature reserve, South China (Mo et al., 2013b). Similarly a
lower mean level of BTBPE at 0.62 (0.07–89) ng/g LW has been reported
in different tissues of water birds from an e-waste recycling facility of
South China (Shi et al., 2009).
Other BFRs such as the novel BFRs (nBFRs) HBB, PBEB, TBBPA and
PBT, etc. have been the least studied in Asian birds. Sun et al. (2014b)
reported very low mean concentrations at 4.45 (nd-10), 0.22 (nd-1.4)
and 0.35 (nd-1.7) ng/g LW for HBB, PBEB and PBT in different terrestrial
species collected from Pearl River delta, South China. In contrast, Zhang
et al. (2011a)reported means concentrations at 15 (0.7–190), 5 (nd-49)
for PBEB and PBT in waterbirds from an e-waste site of South China.
Similarly, A high median level of Tetrabromobisphenol-A (TBBPA)
ranged from 28 to 173 have been reported in six waterbirds species col-
lected from an e-waste recycling region of South China (He et al., 2010)
Likewise, polybrominated biphenyls (PBBs) which have been used since
the middle of the 20th century (not included in the list of nBFRs) and
were subsequently banned through the Stockholm convention, are re-
ported in very few studies from Asia. Mean concentrations at 58.81
(nd-6800) and 0.50 (nd-6.8) ng/g LW for PBB-153 (a congener of
PBB) and PBT have been recorded in terrestrial passerine birds from
South China, respectively (Sun et al., 2012a). Relatively lower mean
levels of PBB-153 at 0.21 (nd-1.4) ng/g LW have been reported in differ-
ent avian species from yellow river delta, North China (Gao et al.,
2009).Corresponding ranges of 3 to 33 and 3.4 to 82 ng/g LW of PBB
have been reported in liver and eggs of common cormorant from
Japan (Watanabe et al., 2004). The reported data on FRs in general and
nBFRs in particular in Asian birds are scarce and/or absent in most
parts of Asia. Recent studies suggest that these contaminants are rising
in Asian avifauna, particularly in top predators, therefore there is a
need of thorough investigation of nBFRs in the future.
3. Comparison between legacy and emerging contaminants
In this review article, we have discuss historically used legacy
compounds and emerging contaminants as two major categories of
OHCs based on the timescale since they have been used. Principal com-
ponent analysis (PCA) was applied to analyze the occurrence pattern of
the OHCs reported in birds of the Asian continent. Fig. 3 indicates three
different groups of OHCs based on their similarity of occurrence in Asian
birds. PCA has been applied on the log10 transformed values of OHCs
against the countries/regions of the Asia where they have been
420 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
Fig. 3. Orientation of different compounds of organohalogens (OHCs) reported in Asian birds at first two axis of Principal component Analysis (PCA). Groupings obtained through plotting
factors loadings of log10 transformed concentrations of compounds reported for different countries in Asia.
reported. The occurrence pattern of different OHCs in birds has been ob-
tained by plotting the factor loadings of PCA for the respective com-
pounds reported in different parts of Asia. In the Fig. 3, historically
used legacy compounds including pesticides grouped together based
on the similarity of their occurrence levels in Asian birds whereas
flame retardants (FRs) and co-PCBs including PCDD/Fs clustered sepa-
rately on the first two axis of the PCA. No particular trend for tissues, re-
gions, feeding and migratory behaviors has been observed through PCA.
In general, the concentrations of legacy contaminants reported in Asian
birds have been found approximately 1 to N 1000 times higher when
compared to BFRs and other novel contaminants. But this is not true
for all the compounds and/or all the cases because different factors
such as vicinity and level of contaminants sources, parameters related
to species and environment either signally or synergistically affects con-
tamination in birds at different location. From the reported literature it
could be deduced that compounds like PCBs, PBDEs including some FRs
were reported in higher concentrations from heavily industrialized and/
or e-waste recycling regions whereas compounds like DDTs and other
pesticides has been reported in higher concentrations from rural or
sub-urban agricultural areas of Asia (Peng et al., 2015a; Yu et al.,
2014). Differences in the reported levels of legacy and emerging con-
taminants have been found statistically significant (P b 0.001). Further,
legacy contaminants in birds have been reported to a wider extent
throughout Asia with a reasonable number of studies whereas emerging
contaminants have mostly been reported in East Asian countries in few
studies. In recent studies from China, Japan and South Korea, emerging
contaminants in birds have been much emphasized whereas in the
rest of Asian continent data regarding these compounds has rarely
been reported. Although the levels of some legacy POPs such as PCBs
and PCDD/Fs in birds from some of the Asian countries has increased a
little or remain steady during the past decade but still very high con-
centrations of most of the pesticides have been reported in recent
studies (Hong et al., 2014; Yu et al., 2013). Despite ban and/or
regulation actions, legacy contaminants have recently been found
in high concentrations in Asian birds which indicates their continuing
use in agriculture and industry due to less effective management. On
the other hand, emerging contaminants are also on the exponential
rise in industrialized countries of Asia such as China, Japan and Korea
(Hong et al., 2014; Mo et al., 2012; Kunisue et al., 2008), whereas the
data from most of the developing part of Asia is missing. From the re-
ported information, it is predicted that levels of legacy contaminants
such as PCBs and most of the novel contaminants including flame retar-
dants are on the rise and their recent levels are needed to be investigat-
ed in birds and other environmental compartments.
4. Regional differences in Asia
Organohalogen contamination levels in Asian birds have been
reported to a limited extent (mostly East Asian countries). Because of
scarcity and/or absence (for most parts of Northern, western and
South Asian regions) of reported literature, it is difficult to understand
the patterns of organohalogen contamination in birds throughout
Asia, however, a preliminary conclusion could be drawn for some
compounds. The current massive rise in agricultural and industrial ac-
tivities is expectedly increasing the concentrations of organohalogens
in most of the developing parts of Asian continent. In Asia, most of the
reported literature is from China and Japan with very few studies from
South Korea, Pakistan, India, Iran, Turkey and Russia, whereas informa-
tion from the rest of the Asian regions is rare or absent. Levels of
organohalogens varied in different Asian countries and/or region
depending upon the prevalence of potential sources, possibility of
trans-boundary movement and exposure routes for different species.
Maps (Fig. 1&2) indicates the regional patterns of PCB, DDTs and
PBDEs (most frequently reported compounds in Asian birds).
On the Asian continent, PCBs and a variety of OCPs have been exten-
sively used in industrial processes and agricultural production during
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
the past century. Fig. 1 indicates that PCBs and OCPs levels dominated in
Japan followed by South China, Russia, South Korea and South India,
whereas relatively moderate to lower concentrations of PCBs and
OCPs were reported in birds from Turkey, Pakistan, Iran, Philippines,
Vietnam and central and northern parts of China. Elevated concentra-
tions of PCBs in Southern China are evidently associated with rapid in-
dustrialization and large scale e-waste recycling activities (Chen and
Hale 2010). Moderate levels of different OCPs such as DDTs and HCHs
recorded in birds of South China depict the historical discharge of
OCPs as compared to lower recent input in this region (Luo et al.,
2009a). Similarly, the levels of different OCPs are reported in elevated
concentrations in Japan despite the restricted use of these OCPs in
Japan since early 1970. In addition to a very high industrial input, it is
presumed that these OCPs are originating from South Asia and China
and subsequently travel to Japan through atmospheric transport (Choi
et al., 2001b; Kumar et al., 2005). The levels of OCPs were reported
higher in suburban to rural areas in China whereas PCBs were higher
in urban locations of South China (Peng et al., 2015a). Moreover, higher
OCPs levels have been reported in birds of China when compared with
other environmental compartments (Nakata et al., 2005). Recent ele-
vated concentrations of different OCPs, particularly DDTs and HCHs sug-
gest higher agricultural activities in rural and sub-urban regions of
central China (Nakata et al., 2005; Yu et al., 2014). Since the use of
OCPs, particularly of DDTs, has been banned in China since 1983, the re-
cent reported concentrations indicate that OCPs are still used illegally in
most rural to suburban parts of China. In Northern China, both PCBs and
OCPs were reported with similar levels in birds indicating both agricul-
tural and industrial upsurge in Northern China and also possibly due to
migratory behavior of some of the studied species (Chen et al., 2009).
Similarly, elevated concentrations of PCBs and OCPs in South Korea
have been explained through industrial discharge and agricultural ac-
tivities in the region (Choi et al., 2001a). The levels of HCHs are more
prevalent in South Indian birds which is due to greater use of insecti-
cides with higher HCHs contents in this region. PCBs and DDTs were re-
ported with relatively lower concentrations in South India probably
because of more conventional agricultural practices and less industries
(Ramesh et al., 1992; Tanabe et al., 1998). In Russia and Turkey, higher
levels of OCPs than PCBs suggested higher historic use of OCPs but it is
declining following the ban of most of OCPs since 1980s. In Pakistan,
the concentrations of PCBs is lower than DDTs and other OCPs indicating
higher agricultural application of OCPs in recent years (Sanpera et al.,
2003). In most of the Asian countries OCPs and PCBs have been banned
and/or restricted between 1970s to 1990 but the reported high concen-
trations in birds suggest that illegal use of these compounds is still going
on in many Asian countries.
Like PCBs and OCPs many emerging FRs have been used on Asian
continent, but they have been documented on a very limited scale.
Only few studies from Southern, Central and Northern China, and
South Korea with a single study from Pakistan, Turkey and Russia each
are available for comparison. Fig. 2 indicates that PBDEs levels are
higher in far Eastern countries like Japan, South and North China and
Korea, whereas in other parts they are reported in lesser concentrations.
In comparison, HBCDs were higher in birds from South Korea than
Russia, Northern and Southern China, respectively. Hong et al. (2014)
deduced that Concentrations of FRs such as PBDEs and HBCDs in birds
were almost equal to the classical POPs indicating the recent input of
emerging FRs compared to the declining PCBs and other historically
used POPs. Further, concentrations of anti, syn and total DPs was greater
in Northern as compared to Southern China. Whereas DBDPE were
higher in birds from South China. Recently a very high level of FRs has
been reported in birds particularly from South and North China, Korea
and Japan (Hong et al., 2014; Zhang et al., 2011b; Shi et al., 2009;
Kunisue et al., 2008; Chen et al., 2007). The increasing concentrations
of FRs in Southern China are evidently associated with higher e-waste
recycling activities whereas, in addition to higher industrial exhaust,
the greater concentrations of PBDEs in Northern China are also probably
421
due to higher trophic levels of the studied species (Luo et al., 2009a;
Wan et al., 2008; Chen et al., 2007). In Japan and South Korea, elevated
concentrations of these compounds also reflect higher industrial
exhaust of these chemicals in the recent past (Hong et al., 2014;
Watanabe et al., 2004Because of rarity of reported information on
PCBs, OCPs and FRs levels in birds from Gulf States, Russia, Turkey,
South Asian and Indo-Malayan region it is difficult to discuss their future
prospects. However, due to established (in Gulf countries, Turkey and
Russia) and emerging (in countries like Pakistan, India, Bangladesh) in-
dustrial setup an increased levels of legacy POPs, pesticides, industrial
chemicals and emerging FRs is expected in most of the developing
parts of Asia. Whereas in countries like China and Japan these
compounds are already on the rise, not much information has been
documented so far. To sum up, on the Asian continent a huge data gap
exists between the reported and expected prevailing condition of
organohalogens contamination. Filling this gap would help to assess,
evaluate and rectify the effects in the future.
5. Global scenario
In a global perspective, Asia stayed higher in the recent concentra-
tions of most of the legacy contaminants particularly those of pesticides
whereas the emerging contaminants including BFRs has been reported
in lower concentrations from Asian species when compared with the
rest of the world (Chen and Hale, 2010; Letcher et al., 2010). The
distribution of OHCs in birds is largely based on the nature and utility
timescale of the compound, sources of OHCs at the studied locations
and type of species and/or tissues selected. It is noticeable that predato-
ry birds on higher trophic levels have been emphasized in the reported
studies from Europe, Canada and the USA when compared to Asian
literature (Gómez-Ramírez et al., 2014; Guerra et al., 2012; Chen and
Hale, 2010;). Because of the scarcity of reported information from
Asia, we compared the generally reported mean levels of OHCs from
Asia to the rest of the world. In general, current concentrations of histor-
ically used contaminants such as PCBs, DDTs, HCBs, HCHs, co-PCBs,
PCDD/Fs and other pesticides were estimated at 10 to N1000 times
higher in Asian birds as compared to current level in the Western
world. This is mainly because of ongoing traditional agricultural
practices in most of the developing Asian countries and frequent use
of these conventional compounds in industry (Peng et al., 2015a;
Hong et al., 2014). On the other hands, novel contaminants including
BFRs, although lower than those from Europe, USA and Canada, are on
the rise in highly industrialized countries of Asia Such as China, Japan
and Korea (Chen and Hale, 2010). Elevated levels of these compounds
in birds of East Asian countries has been attributed to their surplus
use in the industry, poor waste management and extensive e-waste
recycling activities. Yordy et al. (2013)reported far lower concentrations
in birds belonging to different trophic levels for PCBs, DDTs and PBDEs
from South Carolina (USA) than their concentrations in Asia. Likewise,
the concentrations of PCBs and PBDEs in eggs of a passerine bird species,
great tit (Parus major), from 14 different European countries have been
found lower than N 50% of the reported values from Asian studies (Van
den Steen et al., 2009a). On contrary, Jaspers et al. (2006) reported
higher concentrations of PCBs and PBDEs in seven different bird species
from Belgium which is quite comparable to some of the recently report-
ed studies from Asia. Similarly, the reported concentrations of legacy
and emerging flame retardants in Barn owl (Tyto alba) from Belgium
were also quite equivalent to those of some reported studies from Asia
(Eulaers et al., 2014a). Likewise, Chen and Hale (2010) conducted a
global review of PBDEs in birds and concluded that concentrations
were relatively higher in Europe and USA followed by East Asia. Similar-
ly, a median value at 4350 (330–38,000) ng/g LW of PBDEs in eggs of
peregrine falcons (Falco peregrinus) from Canada were found, which is
comparable to the reported values in Asian predators (Guerra et al.,
2012). The concentrations of BFRs and other novel contaminants
recorded from South China, South Korea and Japan are equivalent to
422 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
and sometimes exceed the concentrations reported in USA, Canada and
Europe. Wherever investigated, very low concentrations of these com-
pounds have been reported in the rest of the Asian regions. This is be-
cause of lower industrial usage of these novel chemicals in developing
parts of Asia, although there is a dire need to investigate their more re-
cent levels in birds in the developing parts of Asia. In global scenario of
OHCs contamination in birds, it is predicted that recent concentrations
of OHCs particularly the BFRs are on the rise in Asian birds and that
they need to be regulated.
6. Tissue specific contamination
In this review article we have included the tendency and pattern of
bioaccumulation of organohalogens in different avian tissues reported
from the Asian continent (Table. S.I. 1, 2). It is established that the levels
of different organohalogens vary in different tissues of birds based on
potential of bioaccumulation, biotransformation, detoxification and
excretion mechanisms in different tissues (Fossi, 1995. Further, it is un-
derstood that due to lipophilic characteristics, organohalogens predom-
inately bioaccumulate in the tissues with higher lipid contents. In birds,
both types of lipids like triglycerides and phospholipids are found hav-
ing different structure, function and distribution in different tissues
and hence affect the accumulation of organohalogens in different
tissues (Boumphrey et al., 1993). For organohalogen quantification in
birds of Asia, muscle (in particular pectoral muscle) tissue has been
most frequently studied followed by egg, liver, kidney, blood etc. In
some studies, tissues like subcutaneous fat and preen gland have also
been studied.
Zhang et al. (2011a) recorded significantly higher levels of PCBs,
DDTs and HCHs in liver and kidney as compared to muscle. Significantly
higher levels of PCDDs and PCDFs in liver tissues as compared to the
muscle of black eared kite and great cormorant have been recorded
(Kubota et al., 2006). Further, an increasing trend of liver: muscle for
PCDDs with increase of chlorine level was observed indicating that
highly chlorinated compounds deposit preferentially in liver (Kubota
et al., 2004). Similarly, higher concentrations of PBDEs and other FRs
were recorded in liver and kidney tissues than muscle of water birds
from an e-waste recycling sites of South China (Shi et al., 2009). Chen
et al. 2013 reported a mean (muscle and liver) of (55 and 42 ng/g LW)
for syn DP, (244 and 213 ng/g LW) for ∑DPs and (193 and 243 ng/g
LW) for anti DP predatory birds of North China. Higher lipid content
explained the higher concentrations of organohalogen in kidney and
liver as compared to muscle because these tissues exhibit no significant
differences for lipid normalized concentrations (Zhang et al., 2011b).
Contrary to these findings, PCBs concentrations among muscles, liver
and kidney have not been found significantly different (although higher
in liver and kidney) reported in different species of birds of prey (except
Eurasian sparrowhawk) from Northern China (Chen et al., 2009). Luo
et al. (2009a) deduced that higher organohalogens levels in muscle
are associated with low metabolic activity when compared to liver. In
predatory birds of South India, a sum of total dioxin like PCBs of
55,831 ng/g LW in liver (Senthilkumar et al., 2001a) and 31,766 ng/g
WW in muscles (Senthilkumar and Kannan, 2001b). Rajaei et al.
(2011) concluded that highly chlorinated PCBs preferentially accumu-
lated in muscle whereas lower chlorinated PCBs were more intended
towards feathers. This has been explained by less tendency of preen
oil to undergo metabolism before secretion, thus remaining with
lower chlorinated PCBs congeners in feathers. They also found that
PCBs congener profiles in muscle and liver were similar and higher
from that of feathers. A significant correlation of PCBs concentrations
for blood vs liver and egg vs blood has been reported in water birds
from Turkey. In this study, Mean HCHs concentrations (ng/g LW)
were highest 530 in preen oil followed by liver 94.75, egg 35.66, blood
11.33 and muscle 5.75 ng/g LW respectively. Interestingly, in the same
study a negative correlation has been reported in PBDEs concentrations
between liver and blood, liver and preen oil and egg and preen gland oil
in different water birds (Kocagöz et al., 2014). In general, levels of
organohalogens were higher in eggs as compared to liver of great
cormorant from Sagami River, Japan. (Kumar et al., 2005). The concen-
trations of ∑non-ortho PCBs were found significantly higher in subcu-
taneous fat (9155 ng/g LW) than egg (4905 ng/g LW) of black tailed
gulls (Choi et al., 2001b). So as a general rule, it is predicted that passive
diffusion to lipid unit depicts the pattern of organohalogen distribution
in avian tissues. Moreover, in most of the reported studies from Asia,
invasive matrices of birds have been emphasized whereas evaluation
of noninvasive matrices has commonly been encouraged in modern
toxicological studies.
7. Influence of dietary exposure and trophic levels
Varying levels of organohalogens have been reported in Asian birds
depending upon the dietary sources, exposure and trophic levels of the
birds. As all of these organohalogens tend to persist in the environment,
bio-accumulate in living tissues and biomagnify through the food chain,
higher concentrations of these OHCs have been reported in top preda-
tors. Feeding ecology and trophic levels of the species also have a pro-
found influence on organohalogen accumulation in birds. Use of stable
isotope δ (15N, 13C) is very useful in ecotoxicology to understand the
dietary exposure and biomagnification of pollutants in the birds and
other wildlife (Jardine et al., 2006) Stable isotope 15N values are higher
for organisms occupying higher trophic levels and are enriched 3–5%
per increase in trophic level. Similarly, another stable isotope δ13C
gives information about the source of dietary carbon and is useful to
trace the feeding locations of the organism (Huang et al., 2013). To
predict the sources and habits of diets and to correlate it with the
organohalogens contamination these two isotopes δ13C and δ15N are
most commonly analyzed in avian tissues.
Peng et al. (2015a) reported that species at higher trophic levels
exhibited greater δ15N concentrations than those which are lower on
the food chain. Yu et al. (2014) found that organohalogens and δ13C iso-
topes were higher in urban than non-urban sites in passerine birds of
China, which might be due to replacement of C3 plants by C4 plants in
urban locations. In different studies on PCBs, DDTs and PBDEs, it has
been reported that the level of δ15N increases with increasing concen-
trations of organohalogens suggesting a correlation of δ15N with trophic
levels (Sun et al., 2012a; Zhang et al., 2011a; Wan et al., 2008). Similarly,
Zhang et al. (2011b) reported a positive correlation between trophic
levels and δ15N as well as dietary sources and δ13C. Moreover, higher
levels of δ15N and δ13C have been recorded in shorebirds as compared
to ducks due to higher trophic position of former birds (Huang et al.,
2013). Behrooz et al. (2009) reported that levels of DDTs and PCBs
were higher in carnivorous birds when compared to omnivorous
birds. They found a consistent increase in organohalogens with trophic
level and hence corroborated the biomagnification organohalogens in
the studied food chain. Ito et al. (2013) recorded a maximum mean of
1810 ng/g LW of POPs at Uwashima Island Japan when tracking seabirds
across the Pacific Ocean towards polluted sites indicating a direct rela-
tionship of POPs accumulation patterns with diet and exposure. Further,
Yu et al. (2013) found that PCBs in predatory species being higher on the
food chain biomagnified and exhibited higher concentrations of 835
(44–71,000) ng/g LW when compared to 59 (23–720) ng/g LW in
prey species. Similarly, Senthilkumar et al. (2002) reported an elevated
mean concentrations of PCBs and Co-PCBs as result of biomagnification
of these compounds in the food chain. Peng et al. (2015b) reported that
insectivorous birds exhibited higher DPs concentrations (mean 16.9)
than omnivorous (6.4 ng/g LW) species. Parallel findings for PBDEs
were reported by Ramesh et al. (1992) and Kunisue et al. (2002)
from India and Russia respectively. It is generally corroborated that
organohalogens being persistent, bioaccumulate more in birds that
have a higher trophic position and are thus positively correlated with
δ15N isotope values, whereas their levels in birds are also associated
with dietary sources and correlated with δ13C isotope values. In modern
 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
toxicological studies, predatory flagship species are commonly used, but
this trend is less observed in Asia. Evaluation of the best indicator
species for different trophic levels and comparing the levels of
organohalogens among them would help to understand the sources,
biomagnification and flow of these pollutants in the Asian environ-
ment. In addition to dietary exposure and trophic transfer, there is
an important and closely associated phenomenon of maternal trans-
fer of organohalogens from female to eggs and subsequently in em-
bryos and hatchlings. In many studies from the European continent
(Verreault et al., 2006; Van den Steen et al., 2009b,c) it has been re-
ported that there is a positive correlation between the concentra-
tions of different organohalogens in the female and the laid eggs,
which culminates at reproductive failures and different associated
problems. To the best of our knowledge, there is only a single reported
study (Tanabe et al., 1986) dealing with the maternal transfer of
organohalogens in birds from Asia. They predicted that higher levels
of female exposure to some congeners of PCBs and p,p′ DDE may
cause chick mortalities and other serious toxicological effects in Adelie
penguin (Pygoscelis adeliae). The maternal transfer of OHCs in birds is
the least emphasized aspect in the reported literature from Asia which
is needed to be addressed in future studies.
8. Migratory behavior and organohalogens
Different levels of organohalogens have been reported in resident
and migratory Asian birds. There are two basic factors that predomi-
nately determine the levels of organohalogens in migratory birds. Firstly
there are the physiological changes that occur due to migration, such as
a drop in the fat levels during migration and/or after breeding thereby
affecting the organohalogen burden depending upon the amount of
fat loss. Secondly, the species may accumulate organohalogens from
their wintering grounds with polluted stopover locations (Kunisue
et al., 2002). Sedentary species that exploit local resources may accumu-
late less organohalogens in their tissues, but largely depending upon the
exposure levels in that location. In contrast, highly mobile migratory
species usually best represent the regional and interregional pattern of
pollutants levels (Chen and Hale 2010).
As mentioned previously, Asia is flanked by three major flyways
thereby containing a large number of migratory species that could be
useful to understand the overall inter-regional pattern of contamination
with organohalogens and other pollutants (Huang et al., 2013; Bamford
et al., 2008). Chen et al. (2007) predicted that the concentrations of
PBDEs in raptors of North China were largely associated with feeding
and migratory habits of the species. Hong et al. (2014) reported a higher
range (285–674,000 ng/g LW) of PCBs in migratory species as compared
to the range (14–131,000 ng/g LW) in resident species of South Korea.
Similarly, a higher relative mean PCBs concentration at 675 has been re-
corded in migratory species as compared to 503 in multiple resident
species from South India (Senthilkumar et al., 1999). Further, Ito et al.
(2013) concluded that changes in the foraging site correspondingly
changes the concentrations of different POPs in the preen gland of sea-
birds. Chen et al. (2009) found that POPs concentrations, particularly
DDTs, are markedly influenced by the migratory habits of raptors spe-
cies in Northern China. Species that stayed for a long time in a polluted
site accumulated higher levels of POPs in their tissues as compared to
seasonally migratory species. Choi et al. (2001a) reported an elevated
levels of DDTs and other OCs in migratory species than those of resident
species from South Korea indicating the greater tendency of POPs to ac-
cumulate (particularly OCs) in the tissue of migratory birds. A relatively
higher PCBs level of 430 ng/g WW was reported in migratory species
when compared to 42 ng/g WW in resident species from South India
(Tanabe et al., 1998). Kunisue et al. (2002) reported relatively higher
concentrations of PCBs in migratory species when compared with resi-
dent species of Lake Baikal, Russia. Hong et al. (2014) reported higher
HCHs levels in resident birds as compared to migratory birds of South
Korea, whereas totally opposite findings have been reported in South
423
India (Tanabe et al., 1998). Huang et al. (2013) reported that contamina-
tion of PBDEs in birds of EAA flyway was lower than those reported from
Black sea–Mediterranean and Mississippi flyways from Europe and
North America respectively. It has been deduced that migratory bird
species of Asia usually accumulate more organohalogens than resident
species, although this is also determined through the specific exposure
of the species. In reported Asian literature, comparisons of
organohalogens levels between migratory (particularly the long range
migratory species) and resident species have been little emphasized.
9. Data gaps and future research directions
On the Asian continent, few review articles have been published in
recent years on the issue of organohalogen contamination, levels,
pattern of bioaccumulation, biomagnification, pathways adopted and
their distribution in various environmental compartments (Yadav
et al., 2015; Li et al., 2014; Sarkar et al., 2008; Ramu et al., 2007).
Although birds have been considered as a part of some review articles,
no comprehensive report on current knowledge and future prospects
of organohalogen levels in birds of this region has been formulated so
far. In most of the published literature from the Asian continent, levels
and trophic transfer of organohalogens have been investigated in differ-
ent avian tissues whereas phenomena like bird's migration, long range
transport and maternal transfer of organohalogens have rarely been
discussed. Most of the reported studies are from China, Japan and
South Korea whereas very few studies have been found from India,
Pakistan, Iran, Turkey and Russia. In the current review, we noticed
that there is a serious shortage on published research on organohalogen
contaminations in birds of Asia. Furthermore, due to limited geograph-
ical and timescale information on OHCs levels in Asian birds, it is diffi-
cult to envisage a specific temporal trend for any group of compounds.
To the best of our knowledge, no data on this issue have been reported
from Gulf States and the Indo-Malayan region. Data from South Asia,
Iran, Turkey and Russia are very small and futile to envisage the pattern
of organohalogens in birds of these regions. Most of the Asian countries
are developing and shifting their agricultural economies to industrial
economies thereby introducing a variety of novel chemicals in the envi-
ronment. But a huge gap exists between the currently available litera-
ture and the actual scenario of organohalogen contamination in this
region. Particularly with reference to birds, even baseline data have
not been documented so far to assess the level of threat faced by the
birds of this region.
Firstly, there is an urgent need to develop baseline data throughout
Asian countries particularly on PCBs, OCPs, DDTs and emerging FRs
like PBDEs and other nBFRs. Asia has a very unique avifauna which
includes the critically endangered vultures of South Asia and a large
number of other predatory species. For future studies we recommend
to extend the research on such flagship species in addition to waterbirds
and passerine birds to assess the current and future implications of
organohalogens contamination. Factors such as, dietary sources, expo-
sure patterns, migratory behaviors along with fat/lipid contents in the
studied tissues should be taken into account while planning future stud-
ies. Maternal transfer of organohalogens in birds is the most neglected
aspect in the Asian studies, therefore we recommend to conduct future
research to evaluate this issue on a priority basis. Further, innovative
approaches through stable isotopes will yield very useful information
regarding the sources and transfer of pollutants between the Asian
regions and/or global pollutants transfer. Further, we encourage the
use of non-invasive matrices (such as feathers and deserted eggs) in
avian toxicological studies, so that they can be applied to critically en-
dangered and other declining species. Future research should be fo-
cused on South Asian countries like Pakistan, India and Bangladesh
where organohalogens are expected to be rising due to industrial and
urban expansion. Moreover, intensive research in highly industrialized
countries like China, Japan, South Korea, Turkey, Russia and Gulf States
is required to envisage the future prospects of organohalogens.
424 N.A. Abbasi et al. / Science of the Total Environment 542 (2016) 411–426
Secondly, there is a need to enhance the scientific capacities in Asia
in terms of laboratories, equipment and academia to negotiate the
future implications of exposure and subsequent bioaccumulation of
these contaminants in birds. It is very important to predict the level of
threat that the already declining avifauna of the Asian region is going
to face in the near future due to ongoing organohalogen contamination.
And lastly, it is necessary to initiate proactive campaigns through public
and private sector involvement, encouraging alternatives, awareness
and precautionary measures to avoid future worst scenarios, which
include the extinction of many important avian and other wildlife
species of this region.
10. Conclusion
Levels of organohalogens including legacy POPs and emerging FRs
are likely on the rise due to industrial booming in most parts of the
Asia. However, data on organohalogen contamination in birds of this re-
gion is presently too scarce to assess the levels, distribution and future
implications. Most of the available data is from far East Asian countries
such as China, Japan and South Korea while minor data has been docu-
mented for India, Pakistan, Iran, Turkey and Russia. From the reported
literature we infer that historically used legacy POPs, particularly PCBs
and DDTs have been reported in elevated concentrations in China,
Japan and South Korea, while HCHs were most prevalent in Indian spe-
cies. Moderate levels of all the organohalogens have been reported in
Pakistan, Iran and Turkey. FRs have also been reported with rising
trends in birds of South and North China, Japan and South Korea. Factors
such as, dietary sources, maternal transfer, exposure patterns, migratory
behaviors along with fat/lipid contents in the studied tissues are the key
factors responsible for differences in levels of organohalogens in differ-
ent species. These factors should be taken into account for future studies
and thus a careful planning for forthcoming research is required. We
recommend that future focus should be given towards pollutants such
as PCBs, OCPs, PBDEs and nBFRs in predatory and aquatic indicator spe-
cies with more emphasis on the best use of non-invasive matrices for
obtaining desired results. The unique avifauna of South Asia needs to
be studied on an urgent basis whereas detailed research is needed
from highly industrialized countries, particularly in countries where
no data is available so far.
Conflict of interest
The authors declare full responsibility for any conflict of interest
regarding the funding, preparation and publication of this work.
Acknowledgments
The author is highly thankful to all of co-authors for their assistance
in preparation of this manuscript. Special thanks to the Higher
Education Commission for the support of the doctoral research of
Naeem Akhtar Abbasi at Quaid-i-Azam University, Islamabad,
Pakistan. Dr. Veerle Jaspers is supported by Norwegian University
of Science and Technology (NTNU), Norway. Dr. Tomasz Ciesielski
is acknowledged for sharing literature from Russia. The authors are
also highly thankful to the handling editor Dr. Adrian Covaci and
two anonymous reviewers for their constructive comments that
considerably improved an earlier version of the manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.scitotenv.2015.10.088.
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