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Biodivers Conserv (2010) 19:1063–1082

DOI 10.1007/s10531-010-9778-0

ORIGINAL PAPER

Impacts of pollution on marine life in Southeast Asia

Peter A. Todd • Xueyuan Ong • Loke Ming Chou

Received: 14 September 2009 / Accepted: 9 January 2010 / Published online: 2 February 2010
Ó Springer Science+Business Media B.V. 2010

Abstract Pollutants, originating from both land and sea, are responsible for significant
lethal and sub-lethal effects on marine life. Pollution impacts all trophic levels, from
primary producers to apex predators, and thus interferes with the structure of marine
communities and consequently ecosystem functioning. Here we review the effects of
sediments, eutrophication, toxics and marine litter. All are presently major concerns in
Southeast Asia (SE Asia) and there is little indication that the situation is improving.
Approximately 70% of SE Asia’s human population lives in coastal areas and intensive
farming and aquaculture, rapid urbanization and industrialisation, greater shipping traffic
and fishing effort, as well as widespread deforestation and nearshore development, are
contributing towards the pollution problem. As SE Asia encompasses approximately 34%
of the world’s reefs and between a quarter and a third of the world’s mangroves, as well as
the global biodiversity triangle formed by the Malay Peninsular, the Philippines, and New
Guinea, the need to reduce the impacts of marine pollution in this region is all the more
critical.

Keywords Coral reef  Eutrophication  Mangrove  Marine litter  Seagrass 


Sediment  Toxics

Introduction

For this review we define Southeast Asia (SE Asia) as Brunei Darussalam, Cambodia, East
and West Malaysia, Indonesia, Lao PDR (the only landlocked country), Myanmar, Phil-
ippines, Singapore, Thailand, Timor-Leste, and Vietnam. The region extends over
6,500 km from east to west and 3,500 km from north to south and borders the Gulf of
Thailand, the Andaman Sea, the South China Sea, and the Pacific Ocean. Indonesia and the
Philippines alone comprise over 24,000 islands and more than 70% of SE Asia’s human

P. A. Todd (&)  X. Ong  L. M. Chou


Marine Biology Laboratory, Department of Biological Sciences, National University of Singapore,
14 Science Drive 4, Blk S1 #02-05, Singapore 117543, Singapore
e-mail: dbspat@nus.edu.sg

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population lives in coastal areas (Bryant et al. 1998). Maritime activities are prominent, as
evidenced by the megaports of Manila, Singapore, and Jakarta, and numerous major
shipping lanes (UNEP 2002).
The nearshore waters of SE Asia host approximately 34% (*100,000 km2) of the
world’s reefs (Tun et al. 2004) and between a quarter and a third (*50,000 km2) of the
world’s mangroves (FAO 2007). At its heart is the triangle formed by the Malay Penin-
sular, the Philippines, and New Guinea: a global biodiversity hotspot where most tropical
marine groups have their greatest density of species (Briggs 1999). However, over 80% of
SE Asia’s reefs are at risk (Bryant et al. 1998) and, as highlighted by Spalding et al. (2001,
p. 259), ‘‘burgeoning human populations are over-utilizing the resources in many areas,
while wholesale destruction of the forests on land, together with rapid urbanization, is
leading to massive loads of sediments and pollution’’ .
Marine pollution comes from both land (e.g., via rivers and wind) and sea (e.g., through
marine dredging, mining, dumping and shipping). We will review the effects of sediments,
eutrophication, toxics and marine litter (Table 1) as these are especially pertinent to SE
Asia. Other pollutants, such as heat from industrial cooling effluents, or munitions
dumping, are relatively minor and there is almost no literature for the region. Acidification
and climate change will also not be discussed as these operate at global scales with little
local data for SE Asia. Even though we will touch on most major marine fauna and flora,
the focus will be generally on corals, seagrasses and mangroves which, if not unique to SE
Asia, are more biodiverse here than in any other region.

Sediments

Input of sediments to the sea can be due to natural and anthropogenic processes originating
from both terrestrial and marine environments. Rivers have deposited silts and clays for
millennia however, poor management of agricultural land, dredging and mining activities,
deforestation, and inland construction work can greatly increase sediment loads (Hodgson
1993; Fabricius 2005). All these activities are prevalent in SE Asia. For instance, Thailand,
Indonesia and Malaysia are major tin ore exporting countries and much of the mining is
conducted in coastal waters (Chansang 1988). The quantities of sediments removed are vast:
even in the 1970s dredges could remove over a million cubic meters in 6 weeks’ operation
(Sujitno 1977). The many-fold increase in sediments in Manila bay has contributed to its
position as a pollution ‘‘hotspot’’ in the Philippines (Maria et al. 2009) and suspended
materials originating from land reclamation activities and dredging of shipping lanes con-
tinues to be Singapore’s biggest marine pollution issue (Dikou and van Woesik 2006).
Sediment input and diversity are closely linked. Goh and Chou (1992) found lower live
coral cover at reefs closer to Singapore and attributed their observations to the disparity in
sedimentation rates among sites. They also observed differences in species composition,
including a trend towards more sediment-tolerant taxa closer to Singapore’s main island
where levels were higher (up to 44.64 mg cm2 d-1, as compared to 7.50 mg cm2 d-1 or
below at the site furthest offshore; Low and Chou 1994).
Sedimentation tolerances greatly vary among species of all marine groups, including
Polychaeta, Crustacea, Mollusca, Echinodermata, Hydroida, Porifera, Anthozoa, Bryozoa,
Cirripedia and Ascidiacea (Olsgard and Hasle 1993; Saiz-Salinas and Urkiaga-Alberdi
1999) as well primary producers such as algae (Airoldi and Cinelli 1997) and seagrasses
(Erftemeijer and Lewis 2006). Such differential responses lead to changes in community;
Airoldi and Cinelli (1997, p. 269) observed that ‘‘small scale variations in sedimentation

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Table 1 Summary of pollutants, their sources/causes, and their effects on marine life
Pollutant Sources/causes Effects

Sediment
Terrigenous Agricultural runoff. Deforestation. Construction Reduces light and thus reduces
sites photosynthesis in corals and
Marine Near shore mining. Dredging. Offshore seagrasses. Impacts on visual
construction sites predators and prey. Smothers
benthic organisms. Reduces
suitable substrate for settling larvae
Eutrophication
Nitrogen and Untreated human and animal waste. Industrial Jellyfish blooms. Phytoplankton
phosphorus discharge blooms leading to hypoxia.
Macroalgae blooms that can
outcompete seagrasses and corals.
Increases severity of coral diseases.
Reduces fertilization success in
corals
Toxics
Organochlorine Industrial discharge. Atmospheric deposition Bioaccumulate in marine organisms.
compounds from incineration. Leaching from dumpsites. Decrease reproductive capabilities
Pesticides and pose immunotoxic risk in
marine mammals. Interfere with
hormonal and nervous systems of
marine organisms and humans
Compounds from Accidental oil spills and deliberate operational Bioaccumulate in marine organisms.
oil discharge. Terrestrial runoff from vehicles and Carcinogenic. Disrupt cellular and
industries. Burning of waste and forests biochemical functions
Butyltin Antifouling paint Bioaccumulate in marine organisms.
compounds Cause imposex in gastropods and
(BTs) bivalves. Endocrine disruption in
fishes, marine mammals and
humans
Heavy metals Mining. Vehicle emissions. Leaching from Inhibit recruitment, fertilization and
landfills. Discharge from manufacturing development in various marine
plants. Untreated human and agricultural invertebrates including corals,
waste molluscs and crustaceans
Polybrominated Flame retardants in polymer products Interfere with neurological and
diphenyl ethers hormonal functions
(PBDEs)
Cyanide fishing Live fish trade Coral bleaching and impaired
calcification of skeletons. Kills
various reef-associated organisms
Marine litter
Micro-plastics Resin pellets. Fragments from larger objects Ingestion leading to internal
(\5 mm) blockages and toxic poisoning
Macro-plastics Discarded end-user products Entanglement leading to drowning,
([5 mm) suffocation, and/or starvation due
Lost and Fishing activities to interference with feeding.
abandoned Ingestion leading to internal
fishing gear blockages, toxic poisoning, and/or
(LAFG) starvation due to false ‘stomach
filling’

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rates significantly influenced the local structure and diversity of the algal assemblage’’.
Examples from SE Asia include an altered seagrass community in Calancan Bay, Phil-
ippines, affected by the input of mine tailings (Fortes 1988) and a drop in mollusc species
from 171 to 58 in Jakarta Bay, Indonesia, due to high levels of anthropogenic sediment and
sewage (van der Meij et al. 2009).
In her review on the effects of sediment on coral reefs Rogers (1990) suggests that mean
sedimentation levels between 1 and 10 mg cm2 d-1 or suspended sediment levels of
1–10 mg l-1 are commonly found on undisturbed reefs, whereas chronic levels above
these figures can be considered ‘high’. Fabricius (2005) emphasises that sediment type and
local conditions are also critical, with nutrient-rich silts in calm waters being a particularly
stressful combination. Critical rates for other ecosystems are less well established (e.g.,
Ellison 1998). High sediment loads deleteriously affect the marine environment in two
principal ways, either by physically impacting benthic organisms, e.g., through smothering
or by reducing the amount of suitable substrate for settling larvae; and/or by increasing
turbidity thus reducing photosynthesis as well as visibility (Rogers 1990; Erftemeijer and
Lewis 2006). Sediments may also release nutrients and contaminants, the impacts of which
are discussed more generally in the sections ‘‘Eutrophication’’ and ‘‘Toxics’’ later in this
review.

Physical impacts

The effects of smothering are species-dependent and vary with particle size and sedimen-
tation rates (e.g., Turk and Risk 1981). If high levels of sediments kill the existing fauna
opportunistic species such as polychaetes are likely to predominate (Olsgard and Hasle
1993), and may well become the main component of the biota if excessive sedimentation
continues (Mirza and Gray 1981). Smothering and subsequent decomposition of macroalgae
changes the chemical composition of bottom sediments and this can lead to significant
reductions in meiofaunic diversity and abundance (Neira and Rackemann 1996).
The physical smothering of a coral increases relative respiration due to energy being
diverted into clearing activities. ‘‘All corals exposed to sediments showed an increase in
respiration rate at night and a decrease in net photosynthesis during the day’’ (Abdel-Salam
and Porter 1988, p. 285). Potential food is lost through disruption of prey capture and
greater mucus production equates to a carbon deficit—although some of the energy loss
might be compensated for if the sediment can be utilised as a food source (Stafford-Smith
1993; Riegl and Branch 1995; Anthony and Fabricius 2000). Extreme sediment loads can
lead to burial and eventual mortality (Rogers 1983; Stafford-Smith 1992). Corals can reject
sediment and this ability depends upon their morphology and their behaviour (Todd 2008).
Passive sediment rejection is mostly controlled by colony shape, colony orientation, and
water movement (Rogers 1983, 1990; Riegl et al. 1996). Most corals have active sediment
rejection mechanisms that include polyp inflation, ciliary action, mucus entanglement and
tentacular manipulation of particles (Stafford-Smith and Ormond 1992; Riegl 1995).
Seagrasses grow in sediment and are renowned for their ability to trap and bind it (Gacia
et al. 2003), but they are also sensitive to changes in sediment input. Cabaço et al. (2008)
showed that all taxa they reviewed experienced at least 50% mortality after burial with
among-species sensitivity being strongly size-dependent. Leaf size and rhizome diameter
were the best predictors of survival. Mangroves are also associated with sediments, but
they too can die if their aerial roots become buried (Ellison 1998). Again, responses are
species-specific as well as being contingent on the type of sediment and duration of burial
(Fortes 1988; Ellison 1998).

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It has been well established that sediment-covered substrates are not suitable for coral
larvae to settle on (e.g., Bak and Engel 1979; Rogers 1990; Hunte and Wittenberg 1992).
Among corals in Singapore, Dikou and van Woesik (2006) determined a strong inverse
relationship between the rate of sediment deposition and recruitment rates. Under exper-
imental conditions Hodgson (1990) found that no Pocillopora damicornis larvae, a com-
mon brooding coral in SE Asia, would settle on a glass substrate 95% covered in sediment
[1 mm thick. For Acropora digitifera, fertilization and larval survival were reduced in
experimental high (50 and 100 mg l-1) suspended sediment conditions (Gilmour 1999).
Mollusc larvae, such as the abalone, Haliotis diversicolor, are also negatively affected by
deposited sediments (Onitsuka et al. 2008) and it is reasonable to assume that most benthic
organisms that undergo a larval settlement phase would respond similarly.

Increases in turbidity

Light attenuation increases rapidly in turbid waters (Kirk 1977) and, as light decreases, so
does the range in which photosynthesising organisms can grow (e.g., Falkowski et al.
1990). Photosynthesis and calcification are tightly coupled in zooxanthellate scleractinian
corals, with calcification approximately three times lower in darkness than in light (Ka-
waguti and Sakumoto 1948; Gattuso et al. 1999). In Singapore, chronic levels of sedi-
mentation over the last 30–40 years have resulted in underwater visibility being reduced
from 10 m recorded in the early 1960s to a contemporary average of 2 m (Chou 1996).
This has significantly reduced the depth at which reefs can grow; resulting in a coral dead
zone below 6–8 m at all but the ‘best’ sites.
For seagrasses, turbidity does not only affect the host plants but also their associated
epiphytes, microphytobenthos and macroalgae (Erftemeijer and Lewis 2006). It can result
in decreases in biomass, nutrients, Chl-a content, and a range of other photosynthetic
growth parameters (Coles and McKenzie 2004, in Erftemeijer and Lewis 2006). Seagrass
species vary in their ability to cope with sub-minimal light but those with larger below-
ground biomass are generally better able to withstand low irradiance (Erftemeijer and
Lewis 2006). From the seagrasses reviewed by Erftemeijer and Lewis (2006), the Indo-
pacific species Halophila ovalis was the most sensitive to reduced light.
Suspended sediment concentrations of 100–1000 mg l-1 can deleteriously affect fish
hatching success and larval survival (Auld and Schubel 1978); however, Cyrus and Blaber
(1993) showed that fish diversity can be positively related to turbidity—depending on the
level of suitable adaptations within the population. Turbidity can also have a major impact
on the visual ecology of marine animals (e.g. Weiffen et al. 2006) although exactly how
communication and predator–prey interactions are affected remains unknown.

Eutrophication

Eutrophication refers to an increase of nutrients, usually in the form of phosphorus or


nitrogen compounds, into a water body in sufficient quantities to increase primary pro-
duction. It may occur naturally, e.g., as a result of upwelling, or emanate from human
activities—known as cultural eutrophication (Jørgensen and Richardson 1996). More
recently, eutrophication has been used to describe any nutrient loading of anthropogenic
origin. Numerous kinds of terrestrial pollution, including sewage, detergents, and agri-
cultural runoff, lead to hypernutrification and eutrophication when and where they enter
coastal waters (Kenchington 1985; Grigg and Dollar 1990). Marine dredging and disposal

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of waste at sea can also result in nutrient enrichment. Eutrophication is one of the most
prevalent and potentially destructive pollutants in SE Asia. For example, coral biodiversity
in parts of Indonesia is estimated to have been reduced by up to 60% as a result of
enhanced nutrient levels (Edinger et al. 1998).

Causes of eutrophication

Causes of eutrophication include leaching of animal manure from farms (Gerber et al.
2005), fertilizer runoff (Ayoub 1999), waste material from aquaculture (San Diego-
McGlone et al. 2008), atmospheric deposition (Paerl et al. 2002), sewage, and industrial
discharges (UNEP/GRA 2006). In SE Asia, over 80% of sewage is deposited into the sea
untreated; much of it originating from urban slums (Gomez et al. 1990). In Indonesia,
organic pollution emissions into the South China Sea more than doubled between 1980 and
1993 (Chou 2009). With the increasing affluence in the region comes a demand for homes,
hotels and other prime property developments along the coast. Runoff from construction
sites, dredging for marinas, and resort operations can all create eutrophic conditions (San
Diego-McGlone et al. 2008). In bays and harbours with limited circulation, for example
Manila Harbour, eutrophication can be greatly exaggerated (Gomez et al. 1990).
With advances in technology, a growing population, and external demand for SE Asian
produce (USDA 2009), increasing numbers of livestock farms have shifted to intensive
production systems. Most of these farms are located near urban areas, such as in Hanoi,
Bangkok and Manila, as the exporting of meat and procuring of equipment and feed
necessitates a readily accessible location to minimize the cost of production. Animal
manure is therefore seldom channeled back to agriculture fields but is instead discharged
with little or no treatment (Gerber and Menzi 2006). The application of excessive fertilizer
further introduces nitrogen and phosphorus compounds into waterways and eventually the
sea. Inputs from various sources into rivers in Cambodia, Malaysia, Thailand and Vietnam
results in the release of *300,000 t of nitrogen per year (UNEP/GRA 2006). Nitrogen
fertilizers, animal manure, and industrial emissions can also be deposited back into the
marine environment through atmospheric deposition (Boyd and Clay 1998; Paerl et al.
2002).
Aquaculture, including prawn and fish farming, often concentrates large numbers of
animals in a small area causing high releases of nutrients through fecal matter and animal
feed (Boyd and Clay 1998; San Diego-McGlone et al. 2008). ‘‘In general, some 85% of
phosphorus, 80–88% of carbon and 52–95% of nitrogen input into a marine fish culture
system as feed may be lost into the environment’’ (Wu 1995, p. 159). Briggs and Funge-
Smith (1994, in Dierberg and Kiattisimkul 1996) estimated that the shrimp ponds
(40,000 ha at that time) in Thailand produced the waste equivalent of between 5% and
11% of the Thai population for nitrogen and phosphorus, respectively. As wild fish stocks
deplete globally the aquaculture industry will continue to grow in SE Asia. Unless prac-
tices improve dramatically, concomitant increases in nutrient input are to be expected.

Impacts of eutrophication

Phytoplankton blooms are symptomatic of eutrophication. Of particular concern in SE Asia


are toxic dinoflagellates such as Alexandrium spp. and Pyrodinium bahamense due to their
ability to cause paralytic shellfish poisoning (PSP). Their toxins are absorbed by filter
feeding bivalves and travel up through the food chain (Corrales and Maclean 1995).
Pyrodinium bahamense population explosions have affected the Philippines, Brunei,

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Indonesia, Malaysia and Thailand in the form of ecologically and economically damaging
‘harmful algae blooms’ (HABs). For instance, between 1991 and 2001 there were 38 HABs
in the Gulf of Thailand alone (PCD, no date). Non-toxic phytoplankton blooms are also
associated with a series of problems including shading effects and clogging of fish gills
(Jørgensen and Richardson 1996). Following a phytoplankton bloom, the decomposition of
massive amounts of algae can deplete oxygen, leading to anoxia and hypoxia and sub-
sequent ‘‘mortality, reduced growth rates, and altered distributions and behaviors of fishes’’
(Breitburg 2002, p. 767). Echinoderms and crustaceans are less sensitive to hypoxia than
fish, but more sensitive than annelids and molluscs (Gray et al. 2002).
For corals, that generally grow in oligotrophic waters, elevated nutrient levels are
correlated with the severity of diseases (Bruno et al. 2003), reduced fertilization success
(Harrison and Ward 2001), reduced settlement rates (Hunte and Wittenberg 1992) and
bioerosion by sponges, bivalves and worms (Holmes et al. 2000). Nutrient enhancement
can also cause shifts in competitive advantage towards species that out-compete corals.
Algae respond with accelerated growth, which can smother colonies (Walker and Ormond
1982; Lapointe 1997). Seagrasses are impacted by macroalgae blooms via competition for
nutrients and light (Duarte 1995). Subsequent loss of seagrass leads to an increase in
detritivores, but a decrease in herbivores and macrobenthos diversity (Cardoso et al. 2004).
‘‘The impacts of aquaculture on biodiversity are rarely positive’’ (Beveridge et al. 1994
p. 497) and fish and shrimp farms have been associated with HABs as well as jellyfish
blooms (Purcell et al. 2007), whilst the anoxic areas beneath aquaculture cages can result in
a complete absence of macrobenthos (Beveridge et al. 1994). In Cape Bolinao, the Phil-
ippines, dinoflagellates dominate over diatoms under high nutrition conditions (fish pens),
changing the structure of the phytoplankton community (Yap et al. 2004). Villanueva et al.
(2005, 2006) showed that barnacle growth in Bolinao was enhanced near fish farms,
outcompeting juvenile reef building corals. The corals’ larval metamorphosis and larval
output were diminished and skeletal growth rate reduced by up to 50%.

Toxics

The interconnectedness of water and air has contributed to the pervasiveness of toxin
pollution in the marine environment (Iwata et al. 1994). For instance, organochlorine
compounds, which are associated with industrialization and agriculture, have permeated
even the Arctic (Stern et al. 1997). There is limited information on exposure and envi-
ronmental levels of persistent toxic substances (PTS) in SE Asia as greater focus has been
placed on communicable diseases rather than the health impact of PTS (UNEP 2002).
Gomez et al. (1990) provides an excellent summary of the data available before 1990,
including variations between wet and dry seasons. The level of marine toxin pollution is
expected to rise concurrently with the rapid development of SE Asia (UNEP 2002) and this
process is likely to be exacerbated by increased population growth, especially that
occurring around coastal areas (Sien and Kirkman 2000).
With poverty and weak legislation common in the region, SE Asian countries have
become perpetrators of costal toxin pollution while in pursuit of development and eco-
nomic gains (Tan 2004). For example, driven by the lucrative live coral fish trade, farmers
in the Philippines and Indonesia turned to cyanide fishing despite the obvious unsustain-
ability of the technique, eventually jeopardizing their livelihoods and the food resources
for local communities (McManus et al. 1997). Again, driven by economics, large areas
of forests have been burned to clear land for farming, emitting polycyclic aromatic

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hydrocarbons (PAHs) that eventually end up in the marine environment. Dichlor-


odiphenyltrichloroethane (DDT), which is banned in most developed nations, is still used
by some SE Asian countries to control malaria (Ritter et al. 1997; UNEP 2002). The busy
international shipping routes and harbours in the region have also introduced oil and
endocrine disrupting organotin compounds into the sea (Yang et al. 1998; Swennen et al.
2009).
The activities outlined above, have contributed heavy metals, organometallics, PAHs,
organochlorine compounds, PBDEs, and cyanide to SE Asia’s marine environment. Below,
some the effects of these toxic compounds are discussed.

Organochlorine compounds

Organochlorine compounds are a form of persistent organic pollutant (POP) found ubiq-
uitously in the environment. Their recalcitrant nature allow them to bioaccumulate in
animals, especially in top predators (Bayen et al. 2003), including humans (Wolff et al.
1993). SE Asia is a point source from which many key organochlorine pollutants spread to
the rest of the globe through the process of evaporation and atmospheric deposition (Iwata
et al. 1994). Organochlorine pollutants of key concern in SE Asia include PCBs and
organochlorine pesticides such as DDT, chlordane (CHL), and hexachlorocyclohexane
(HCH).
PCBs are associated with waste discharge from industries, atmospheric deposition from
incineration, and leaching from dumpsites. As a result, they are usually found at higher
concentration in industrialized areas (Kennish 1997). In SE Asia, PCB concentrations are
relatively low in Cambodia, Indonesia, Malaysia and Vietnam as compared to other
industrialized nations in Asia; Japan and Russia for example (Monirith et al. 2003).
However, within-country hot spots do exist, including Manila, Bangkok and western
Singapore (Kan-atireklap et al. 1997; Wurl and Obbard 2005).
Global environmental measures suggest that the marine environment serves as a major
PCB sink (National Research Council 1979; Tanabe 1985). Correspondingly, marine
animals are more exposed, and thus particularly at risk susceptible, to PCB pollution
(Tanabe 1988). In the tropics, the sinking rate of PCBs from the surface to deeper parts of
the ocean is slower compared to higher latitudes, extending the period of contamination
(Tanabe 1985). PCB levels in gill-breathing marine organisms are determined by the
amount of PCBs in the water; however, levels can bioaccumulate to high concentrations in
marine mammals (Tanabe 1988), affecting reproductive capabilities and posing immu-
notoxic risks (Ross et al. 2000). Small cetaceans are especially susceptible to PCB bio-
accumulation due to their reduced capacity to metabolize these chemicals (Tanabe 1988;
Kannan et al. 1989).
High levels of DDT, CHL and HCH are present in the air above the coasts of SE Asia
(Iwata et al. 1994). DDT was first employed as an effective malaria control in the region in
the 1950s and is still used in the Philippines, Thailand and Papua New Guinea. Even
though other SE Asian countries have banned DDT (UNEP 2002) significant levels can be
found in green mussels in Vietnam, Cambodia, Indonesia, and Malaysia (Kan-atireklap
et al. 1997; Monirith et al. 2003). There is limited information on chlordane pollution in the
region, but it is used in the timber industry and as pesticides against termites (UNEP 2002)
and high levels have been established in mussels in Thailand and sediments around the
coast of Singapore (Kan-atireklap et al. 1997; Wurl and Obbard 2005). HCH exist in two
formulations: the technical HCH and Lindane. Technical HCH has been detected in the
river and estuarine waters of Thailand, Indonesia and Vietnam (Kan-atireklap et al. 1997)

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while Lindane was found recently in the sea off Malaysia and in biota around the coast of
Singapore (Wurl and Obbard 2005). The bioaccumulation and biomagnification of pesti-
cides can interfere with hormonal, reproductive and nervous systems in molluscs, crus-
taceans, fishes, shore birds, marine mammals, as well as in humans (Portmann 1975; Wolff
et al. 1993; Frigo et al. 2002).

Compounds from oil

The shipping lanes of SE Asia are among the busiest in the world and associated oil
pollution is found in the Straits of Malacca, South China Sea, Gulf of Thailand, and the
Jakarta-Manila and Singapore-Bangkok routes (Lu 2003). Some measures to regulate oil
residues undertaken by Malaysia and Singapore to control pollution from vessels in the
Strait of Johore have been quite successful (Gomez et al. 1990). While accidental oil spill
incidences receive much public scrutiny, the majority (almost 10 times more) of oil in the
sea comes from deliberate operational discharge (Lu 2003). In addition, automobiles, street
dust and various industries contribute via terrestrial runoff and atmospheric deposition
(Yang et al. 1998; Boonyatumanond et al. 2006; Song 2008). Many substances in crude oil
are toxic and of a particular concern are PAHs.
Zakaria et al. (2002) and Isobe et al. (2007) suggest widespread input of petrogenic PAH
into SE Asia’s coastal waters. They are especially persistent ([20 years) in mangroves due
to the high organic content of mangrove sediments which readily adhere to PAHs (Evans
et al. 1990; Burns et al. 1994; Liang et al. 2007). Mangrove ecosystems retain PAHs where
they bioaccumulate, disrupting cellular and biochemical functions by binding with DNA
and proteins (Varanasi et al. 1989). The burning of waste and forest fires are major sources
of pyrogenic PAHs. Such activities are common in SE Asia (e.g.; Siegert and Hoffmann
2000; Herawati et al. 2006; Taylor 2010) but PAH emission data are scarce.

Butyltin compounds (BTs)

Antifouling paint on ship hulls also pollutes the sea with BTs: mono- (MBT), di- (DBT)
and tri-butyltins (TBT), which all have detrimental impacts on marine organisms. BTs are
endocrine disruptors, causing ovarian spermatogenesis in oysters, and imposex (imposition
of male genitalia on female, leading to sterilization of females) in gastropods and bivalves
(Horiguchi 2006). Occurrence of imposex has been recorded throughout most of SE Asia,
including Singapore, Malaysia, Indonesia, and Thailand, with extremely high levels
reported in areas with high shipping activities (Ellis and Agan Pattisina 1990; Kan-
atireklap et al. 1997; Kannan et al. 1995; Swennen et al. 2009). In addition to sterilization
of females, BTs are also known to induce shell deformities in oysters (Alzieu et al. 1989)
and TBT-containing antifouling paint can affect coral settlement and metamorphosis
(Negri and Heyward 2001). BTs also accumulate in molluscs, fishes and polycheates
(Harino et al. 2005) and are transferred to higher trophic levels, including dugongs and
humans, upon consumption (Harino et al. 2007; Takahashi et al. 1999).

Heavy metals

Large amounts of heavy metals are introduced into the environment from many anthro-
pogenic sources including mining, automobile emissions, leaching from landfills, and
manufacturing (Shazili et al. 2006). Heavy metals include transition metals which are

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sometimes needed in small amount for metabolic activities but are toxic at high concen-
tration; and metalloids which are toxic even at low levels (Kennish 1997).
In Malaysia and Thailand, extremely high level of lead (Pb) contamination has been
detected in areas with high human activities, such as Johor and Bangkok. Important
sources of Pb pollution include leaded petrol and direct dumping of industrial and domestic
waste (Menasveta and Cheevaparanapiwat 1981; Shazili et al. 2006). In Indonesia, rela-
tively high levels of Pb, cadmium (Cd), copper (Cu), tin (Zn), nickel (Ni) and iron (Fe)
have also been found in sediments that are receiving outflow from industrial areas (Amin
et al. 2009). The direct discharge of effluent from pig farms in west Malaysia contaminate
the costal biota and sediments with high concentration of Cu and Zn, which is added to the
pigs’ diet (Ismail and Ramli 1997). Cu can inhibit a wide range of coral functions including
recruitment, fertilization and development (Reichelt-Brushett and Harrison 1999; Reichelt-
Brushett and Harrison 2000). Pb and Cd affect development of economically important
oysters and mud crabs cultivated in Malaysia (Ramachandran et al. 1997).

Polybrominated diphenyl ethers (PBDEs)

PBDEs are used as flame retardants in polymer products, especially electronics. They are
introduced into the environment throughout the lifetime of the product, from its synthesis
to disposal (DEPA 1999). They are known to interfere with neurological (Viberg et al.
2002) and hormonal (Zhou et al. 2002) functions, but their effects on marine organisms are
not well studied.
Much of the world’s discarded PBDE-containing manufactured goods are disposed in
East and SE Asia, posing a significant source of PBDE pollution in this region. A relatively
high profile example is the export of electronic waste from Japan to Thailand as part of an
economic partnership agreement (Macan-Markar 2007). PBDEs from old electronic
components enter the atmosphere and eventually deposit into the water where they persist
in marine animals. PBDEs are ubiquitous in the marine environment of Singapore (Bayen
et al. 2003) but there is little information on PBDE pollution for elsewhere in SE Asia.

Cyanide fishing

Cyanide is used to stun and capture reef fishes to supply the lucrative live ornamental and
food fish trades. Cyanide fishing started in the 1960s in the Philippines and has spread to
Indonesia, Thailand, and Malaysia (Bryant et al. 1998; McManus 1997). Cyanide impairs
photosynthesis in coral’s symbiotic zooxanthellae by crippling the photosynthetic electron
transport system. This leads to expulsion of the zooxanthellae by the host following
cyanide exposure (Jones et al. 1999; Jones and Steven 1997). It also affects calcification of
coral skeletons (Chalker and Taylor 1975) and can cause tissue to slough off (Cervino et al.
2003). The consumption of reef fish in Asia has surpassed the sustainable production in SE
Asia by six times, posing as a serious threat to the food resource of local communities
(Warren-Rhodes et al. 2003) and well to the ecology of coral reefs.

Marine litter

Marine litter includes any solid waste of anthropogenic origin that ends up in the sea,
whether deliberately or unintentionally. Input amounts to millions of tonnes per year
(UNEP 2005) and globally plastics, debris, garbage, decommissioned structures, vessels

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and vehicles, plus lost and abandoned fishing gear (LAFG) have been accumulating in the
oceans. It kills marine animals directly through entanglement (leading to drowning, suf-
focation, and/or starvation due to interference with feeding) and ingestion (leading to
internal blockages, toxic poisoning, and/or starvation due to false ‘stomach filling’) and
can also affect ecosystems and biodiversity by acting as transport for invasive species
(Derraik 2002; Barnes 2002) or smothering benthic fauna (Uneputty and Evans 1997b).
There is currently little research regarding the extent of marine litter in SE Asia and its
impact on marine biodiversity, although some studies have highlighted the problem (e.g.,
Evans et al. 1995; Uneputty and Evans 1997a, b; Willoughby 1986; Willoughby et al.
1997). What is known is that the amount of marine litter generated by SE Asia nations
equals or exceeds global averages (UNEP EAS/RCU 2008). This can be attributed to
massive urban and industrial development in the region’s coastal areas, intense shipping
activity, and the absence of effective prevention and control measures.Volunteer coastal
cleanup campaigns provide a indication of the extent of the problem, for example, in
September 2009 eight mangroves (1.1 km of coast) in Singapore yielded almost forty
thousand items of litter altogether weighing over five tonnes (ICCS 2009).
Surprisingly, the urgent need to address the issue of marine litter is only in recent years
being considered (UNEP 2009) with a concerted call for stronger enforcement of laws and
regulations, greater awareness campaigns and the use of more effective economic instru-
ments and incentives. The lack of coordinated global and local strategies was identified as
contributory to the persistence of solid waste in the marine environment and led to the
formation of the UNEP Global Initiative on Marine Litter. It has since organised and
implemented activities around the world, particularly in the twelve regional seas of UNEP.
Here we will examine in more detail two major components of marine litter: plastics and
LAFG, as they are the main killers of marine life; the former because of their ubiquity and
persistence and the latter because trapping organisms is what fishing gear is designed for.

Plastics

Plastic pollution accounts for approximately 60–80% of marine litter (Moore 2008). It can
be categorized into two main types: end-user products such as plastic bottles, bags,
packaging, etc., and small resin (e.g., polypropylene and polyethylene) granules or pellets
that are used as the raw material by industries making plastic goods (Azzarello and
Vanvleet 1987). Moore (2008) also classes plastics into two categories: ‘macro’ ([5 mm)
and ‘micro’ (\5 mm) but includes both fragments from larger objects as well as resin
pellets under ‘micro’. The amount of time required for plastics to completely biodegrade is
probably in the 100s of years (Moore 2008); they are also often buoyant and this com-
bination leads to tremendous dispersal potential. Marine mammals (Jones 1995), turtles
(Bjorndal et al. 1994), seabirds (Azzarello and Vanvleet 1987; Moser and Lee 1992) and
crustaceans (Laist 1997) seem to be especially vulnerable to plastic marine litter. Seals
with ‘neck collars’ (usually a loop of plastic) are among the more notorious images of
marine litter, but sea turtles, 26 species of cetaceans, and almost half of all seabird species
ingest, or get entangled in, solid plastic waste (Moore 2008). In total ‘‘267 species of
marine organisms worldwide are known to have been affected by plastic debris, a number
that will increase as smaller organisms are assessed’’ (Moore 2008, p. 131).
Benton (1995) surveyed islands in the South Pacific and concluded that even beaches in
remote areas had similar amounts of garbage to those in western Europe. Conversely,
research in eastern Indonesia shows a correlation between beach litter and proximity to
human populations (e.g., Evans et al. 1995). The amount of plastic found in SE Asian

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marine litter is comparable to global figures. For instance, white polystyrene and plastic
bags accounted for, respectively, 38 and 27% of the total beach litter on 23 islands in
Jakarta Bay, Indonesia (Willoughby et al. 1997). In the first research of its kind in the
region, Ng and Obbard (2006) identified particles of polyethylene, polypropylene, poly-
styrene, nylon, polyvinyl alcohol and acrylonitrile butadiene styrene, in seawater and
sediments around the coast of Singapore. They considered these microplastics to be most
likely derived from broken down larger debris, especially the samples from public beaches
where end-user plastic litter is common.
The problem of plastic marine litter in SE Asia seems to be worsening. In a study of the
Pulau Seribu Archipelago to the north and west of Jakarta, Uneputty and Evans (1997a,
p. 654) noted ‘‘amounts of litter on shores have increased substantially since 1985,
presumably reflecting both accumulation of slowly degrading plastics in the coastal
environment and increased use of plastics during the past decade.’’

Lost and abandoned fishing gear (LAFG)

LAFG can be considered a subset of plastics as most modern fishing gear is made from
durable nylon and other synthetic polymers (Azzarello and Vanvleet 1987; Pruter 1987).
By weight, trawl netting, monofilament gillnet, and maritime line are major components of
LAFG (Donohue et al. 2001), but traps, floats, bait packaging, etc., all contribute to this
growing problem. LAFG consists of gear and materials that are either accidentally lost or
intentionally abandoned by fishers. For instance, Jones (1995) wrote that an Australian
Fishing Zone observer estimated that each year approximately 2580 km of monofilament
line was discarded by Japanese longliners fishing around Tasmania. LAFG can make up
the majority of solid waste in some areas, especially further away from dense human
populations and industry (Derraik 2002; Lee et al. 2006).
Impacts include ‘ghost-fishing’ when nets and lines continue to trap and kill both com-
mercial and non-target animals including endangered species such as turtles, marine mam-
mals and seabirds (Laist 1997), physical damage to coral reefs and associated fauna (Donohue
et al. 2001); the transboundary transport of alien fouling species to new habitats; and the
eventual landfall that creates problems for intertidal organisms. Direct economic costs are
incurred when LAFG traps commercially-sought species, vessels become entangled, ame-
nities become affected, and beaches need cleaning up. There are also a number of additional
issues associated with hazardous materials, medical wastes, syringes, glass and other dan-
gerous debris that wash up on shores. The problem of LAFG is likely to increase due to the
economic significance of fisheries and the difficulties involved in regulating them (Jones
1995), especially the illegal, unregulated and unreported fishing common in the region.

Discussion and conclusions

There are three principle dimensions to the pollution problem in SE Asia: the levels of the
pollutants, the geographic distribution of the pollutants, and the biological impact of the
pollutants on local flora and fauna. There exist large knowledge gaps for all three
dimensions as most countries in the region possess or release very little information on
marine pollution, hence why a detailed table of contemporary data for SE Asia is not
provided here. Potential impacts often have to be extrapolated from other tropical, or even
temperate, seas. Better monitoring protocols, greater disclosure, and more scientific
research would provide a stronger basis for management decisions.

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While the effects of some pollutants at ecosystem-level are known, such as ‘com-
pressed’ coral reefs due to turbidity-induced reductions in light penetration and conse-
quently the depth that corals can grow (Fabricius 2005), the larger-scale effects of litter and
toxics, for example, remain poorly understood. Similarly, eutrophication is often highly
spatially and temporally variable, and correlated with numerous other factors, thus pin-
pointing the influence of enhanced nutrient input can be difficult to determine. Studying the
impacts of pollutants on whole ecosystems is obviously challenging, but there this is a
critical need for this research to be undertaken.
Given SE Asia’s position as a global centre of marine biodiversity, the implications of
marine pollution are enormous. It is understood that the fauna and flora of various marine
environments can be resilient to certain levels of impacts (e.g., Mumby et al. 2007);
however, the synergistic effects of many stressors acting simultaneously can be devas-
tating. For SE Asian countries, short-term economic gain may seem more important than
protecting of the environment; this attitude must change if pollution levels are to be
controlled. At the national level, action is needed to sustain awareness campaigns targeting
industry, community and government groups, as well as integration of marine pollution
concerns into existing conservation strategies, development of pollution trajectory models,
and establishment of monitoring and assessment protocols. As suggested by Derraik (2002,
p. 848) a ‘‘combination of legislation and the enhancement of ecological consciousness
through education is likely to be the best way to solve such environmental problems’’.
Farming and aquaculture-associated pollution issues, including sediments, nutrients and
pesticides, can be ameliorated by showing farmers how they can optimise their yield
without compromising the environment (Wu 1995; Boyd and Clay 1998). That drink-can
detachable ring pulls have been replaced by stay-on-tabs and six-pack yokes are now less
common or at least rapidly photodegradable provides hope that manufacturers can take the
initiative and make their products more wildlife-friendly. Environmental impact assess-
ments (EIAs) are now required by most SE Asian countries before development projects
can commence (Gomez et al. 1990). With the International Convention on the Control of
Harmful Anti-fouling Systems on Ships, 2001, the use of TBT has declined (Bray 2006)
and, as awareness of chemical pollutants grows, new legislation to ban the worst toxics can
be anticipated. Even in developed countries, however, getting land-based polluters to
consider their effect on the marine environment is difficult, and this may therefore be one
of the greatest problems facing SE Asia.
Numerous international conventions designed to protect the seas from pollution have
been signed by one or more (but never all) SE Asian nations, including the International
Convention for the Prevention of Pollution from Ships (MARPOL), Convention on the
Prevention of Marine Pollution by Dumping of Wastes and Other Matter, Protocol Relating
to Intervention on the High Seas in Cases of Pollution by Substances other than Oil; plus
other, more general, conservation conventions such as the ASEAN Agreement on the
Conservation of Nature and Natural Resources, the Convention on Fishing and Conser-
vation of the Living Resources of the High Seas, and the Convention on Biological
Diversity. Of these the most important is probably MARPOL (Derraik 2002) and, if SE
Asia, or at least the South China Sea, could be made a ‘‘special area’’ under this agreement
it could expect more protection than other regions. Of course, as with all such agreements,
there need to be the political will to implement and enforce the guidelines.
Compounding the pollution issue is the region’s rich marine biodiversity, which makes
it all the more urgent for implementation of effective management measures. The eco-
nomic losses associated with excess sediments, eutrophication, toxics and marine litter in
terms of impact on fisheries, human health and tourism should be enough to stimulate

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prevention measures (as opposed to damage control) but once the ecological goods and
services provided by healthy and biodiverse marine systems are factored in there can really
be no excuse to ignore marine pollution. A strong message has to be conveyed that marine
life in SE Asia is experiencing huge environmental stress and inaction will inevitably lead
to habitat degradation, local extinctions, and widespread ecological failure.

Acknowledgements Many thanks to Lian Pin Koh and Navjot Sodhi and for inviting us to write this
article. The authors gratefully acknowledge the support & contributions of the Singapore-Delft Water
Alliance (SDWA). The research presented in this work was carried out as part of the SDWA’s Marine &
Coastal Research Programme (Theme 2): ‘‘Dredging and infrastructure development near critical marine
ecosystems’’ (R-264-001-001-272). We also thank Christina Belle for proof-reading and input; and the
reviewers for their comments and constructive criticism. The Marine Biology class of Spring 2009 kindly
provided many useful references.

References

Abdel-Salam HA, Porter JW (1988) Physiological effects of sediment rejection on photosynthesis and
respiration in three Caribbean reef corals. Proc 6th Int Coral Reef Symp 2:285–292
Airoldi L, Cinelli F (1997) Effects of sedimentation on subtidal macroalgal assemblages: an experimental
study from a Mediterranean rocky shore. J Exp Mar Biol Ecol 215:269–288
Alzieu C, Sanjuan J, Michel P, Borel M, Dreno JP (1989) Monitoring and assessement of butyltins in
Atlantic coastal waters. Mar Pollut Bull 20:22–26
Amin B, Ismail A, Arshad A, Yap CK, Kamarudin MS (2009) Anthropogenic impacts on heavy metal
concentrations in the coastal sediments of Dumai, Indonesia. Environ Mon Assess 148:291–305
Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under
varying turbidity. J Exp Mar Biol Ecol 252:221–253
Auld AH, Schubel JR (1978) Effects of suspended sediment on fish eggs and larvae: a laboratory assess-
ment. Estuar Coast Mar Sci 6:153–164
Ayoub AT (1999) Fertilizers and the environment. Nutr Cycl Agroecosyst 55:117–121
Azzarello MY, Vanvleet ES (1987) Marine birds and plastic pollution. Mar Ecol Prog Ser 37:295–303
Bak RPM, Engel MS (1979) Distribution, abundance and survival of juvenile hermatypic corals (Sclerac-
tinia) and the importance of life history strategies in parent coral community. Mar Biol 54:341–352
Barnes DKA (2002) Biodiversity: invasions by marine life on plastic debris. Nature 416:808–809
Bayen S, Thomas GO, Lee HK, Obbard JP (2003) Occurrence of polychlorinated biphenyls and polybro-
minated diphenyl ethers in green mussels (Perna viridis) from Singapore, Southeast Asia. Environ Tox
Chem 22:2432–2437
Benton TG (1995) From castaways to throwaways: marine litter in the Pitcairn Islands. Biol J Linn Soc
56:415–422
Beveridge MCM, Ross LG, Kelly LA (1994) Aquaculture and biodiversity. Ambio 23:497–502
Bjorndal KA, Bolten AB, Lagueux CJ (1994) Ingestion of marine debris by juvenile sea turtles in coastal
Florida habitats. Mar Pollut Bull 28:154–158
Boonyatumanond R, Wattayakorn G, Togo A, Takada H (2006) Distribution and origins of polycyclic
aromatic hydrocarbons (PAHs) in riverine, estuarine, and marine sediments in Thailand. Mar Pollut
Bull 52:942–956
Boyd CE, Clay JW (1998) Shrimp aquaculture and the environment: an adviser to shrimp producers and an
environmentalist present a prescription for raising shrimp responsibly. Scientific American Magazine.
Scientific American Inc, New York, pp 59–65
Breitburg D (2002) Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes
and fisheries. Estuaries 25:767–781
Briggs JC (1999) Coincident biogeographic patterns: Indo-West Pacific Ocean. Evolution 53:326–335
Briggs MRP, Funge-Smith SJ (1994) A nutrient budget of some intensive marine shrimp ponds in Thailand.
Development of strategies for sustainable shrimp farming. Final report to the Overseas Development
Administration, Research Project R4751. Institute of Aquaculture, University of Stirling, UK
Bruno JF, Petes LE, Harvell DC, Hettinger A (2003) Nutrient enrichment can increase the severity of coral
diseases. Ecol Lett 6:1056–1061
Bryant D, Burke L, McManus JW, Spalding M (1998) Reefs at risk—a map-based indicator of threats to the
world’s coral reefs. World Resources Institute, International Center for Living Aquatic Resources

123
Biodivers Conserv (2010) 19:1063–1082 1077

Management, World Conservation Monitoring Centre and United Nations Environment Programme,
pp 56
Burns KA, Garrity SD, Jorissen D, MacPherson J, Stoelting M, Tierney J, Yelle-Simmons L (1994) The
Galeta oil spill. II. Unexpected persistence of oil trapped in mangrove sediments. Estuar Coast Shelf
Sci 38:349–364
Cabaço S, Santos R, Duarte CM (2008) The impact of sediment burial and erosion on seagrasses: a review.
Estuar Coast Shelf Sci 79:354–366
Cardoso PG, Pardal MA, Lillebø AI, Ferreira SM, Raffaelli D, Marques JC (2004) Dynamic changes in
seagrass assemblages under eutrophication and implications for recovery. J Exp Mar Biol Ecol
302:233–248
Cervino JM, Hayes RL, Honovich M, Goreau TJ, Jones S, Rubec PJ (2003) Changes in zooxanthellae
density, morphology, and mitotic index in hermatypic corals and anemones exposed to cyanide. Mar
Pollut Bull 46:573–586
Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in
calcification of the coral Acropora cervicornis. Proc Roy Soc Lond B 190:323–331
Chansang H (1988) Coastal tin mining and marine pollution in Thailand. Ambio 17:223–228
Chou LM (1996) Response of Singapore reefs to land reclamation. Galaxea 13:85–92
Chou LM (2009) The East Asian seas state of the marine environment report. UNEP EAS/RCU, Bangkok
Coles R, McKenzie L (2004) Trigger points and achieving targets for managers. Paper presented at a
workshop session on management issues during the ISBW-6 Workshop, Seagrass Conference,
Townsville
Corrales RA, Maclean JL (1995) Impacts of harmful algae on seafarming in the Asia-pacific areas. J App
Phycol 7:151–162
Cyrus DP, Blaber SJM (1993) Turbidity and salinity in a tropical northern Australian estuary and their
influence on fish distribution. Estuar Coast Shelf Sci 36:545–563
DEPA (1999) Brominated flame retardants: substance flow analysis and assessment of alternatives. Envi-
ronmental Project 494, Danish Environmental Protection Agency
Derraik JGB (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull
44:842–852
Dikou A, van Woesik R (2006) Survival under chronic stress from sediment load: spatial patterns of hard
coral communities in the southern islands of Singapore. Mar Pollut Bull 52:7–21
Donohue MJ, Boland RC, Sramek CM, Antonelis GA (2001) Derelict fishing gear in the Northwestern
Hawaiian Islands: diving surveys and debris removal confirm threat to coral reef ecosystems. Mar
Pollut Bull 42:1301–1312
Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:
87–112
Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and coral biodi-
versity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over
time. Mar Pollut Bull 36:617–630
Ellis DV, Agan Pattisina L (1990) Widespread neogastropod imposex: a biological indicator of global TBT
contamination? Mar Pollut Bull 21:248–253
Ellison JC (1998) Impacts of sediment burial on mangroves. Mar Pollut Bull 37:420–426
Erftemeijer PLA, Lewis RRR III (2006) Environmental impacts of dredging on seagrasses: a review. Mar
Pollut Bull 52:1553–1572
Evans KM, Gill RA, Robotham PWJ (1990) The PAH and organic content of sediment particle size
fractions. Wat Air Soil Poll 51:13–31
Evans SM, Dauson M, Day J, Frid CLJ, Gill ME, Pattisina LA, Porter J (1995) Domestic waste and TBT
pollution in coastal areas of Ambon Island (Eastern Indonesia). Mar Pollut Bull 30:105–115
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and
synthesis. Mar Pollut Bull 50:125–146
Falkowski PG, Jokiel PL, Kinzie RA (1990) Irradiance and corals. In: Dubinski Z (ed) Ecosytems of the
World 25: Coral Reefs. Elsevier, Amsterdam, pp 89–107
FAO (2007) The world’s mangroves 1980–2005. FAO Forestry Paper 153. Food and Agricultural Orga-
nization, Rome, Italy, pp 77
Fortes MD (1988) Mangrove and seagrass beds of East Asia: habitats under stress. Ambio 17:207–213
Frigo DE, Burow ME, Mitchell KA, Chiang TC, McLachlan JA (2002) DDT and its metabolites alter gene
expression in human uterine cell lines through estrogen receptor-independent mechanisms. Environ
Health Perspect 110:1239–1245
Gacia E, Duarte CM, Marba N, Terrados J, Kennedy H, Fortes MD, Tri NH (2003) Sediment deposition and
production in SE-Asia seagrass meadows. Estuar Coast Mar Sci 56:909–919

123
1078 Biodivers Conserv (2010) 19:1063–1082

Gattuso J, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and
community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool
1999:39–160
Gerber P, Menzi H (2006) Nitrogen losses from intensive livestock farming systems in Southeast Asia: a
review of current trends and mitigation options. Int Congr Ser 1293:253–261
Gerber P, Chilonda P, Franceschini G, Menzi H (2005) Geographical determinants and environmental
implications of livestock production intensification in Asia. Bioresour Technol 96:263–276
Gilmour J (1999) Experimental investigation into the effects of suspended sediment on fertilisation, larval
survival and settlement in a scleractinian coral. Mar Biol 135:451–462
Goh NKC, Chou LM (1992) A comparison of benthic life-form characteristics of a reef (Cyrene) nearest to
and a reef (Raffles Lighthouse) furthest from mainland Singapore. Third ASEAN Science and Tech-
nology Week Conference Proceedings 6:55–62
Gomez ED et al (1990) State of the marine environment in the East Asian Seas Region. UNEP Regional
Seas Reports and Studies No. 126
Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine
environment. Mar Ecol Prog Ser 238:249–279
Grigg RG, Dollar SJ (1990) Natural and anthropogenic disturbance on coral reefs. In: Dubinski Z (ed)
Ecosystems of the World, 25: Coral Reefs. Elsevier, Amsterdam, pp 439–452
Harino H, O’Hara SCM, Burt GR, Chesman BS, Langston WJ (2005) Accumulation of butyltin compounds
in benthic biota of the Mersey Estuary. Mar Pollut Bull 50:222–225
Harino H, Ohji M, Wattayakorn G, Adulyanukosol K, Arai T, Miyazaki N (2007) Concentrations of
organotin compounds in tissues and organs of dugongs from Thai coastal waters. Arch Environ
Contamin Toxicol 53:495–502
Harrison P, Ward S (2001) Elevated levels of nitrogen and phosphorus reduce fertilisation success of
gametes from scleractinian reef corals. Mar Biol 139:1057–1068
Herawati H, Santoso H, Forner C (2006) Forest fires and climate change in Indonesia: Background docu-
ment for the Southeast Asia kick-off meeting of the project Tropical Forests and Climate Change
Adaptation (‘‘TroFCCA’’)
Hodgson G (1990) Sediment and the settlement of larvae of the reef coral Pocillopora damicornis. Coral
Reefs 9:41–42
Hodgson G (1993) Sedimentation damage to reef corals. In: Ginsberg RS (ed) Proceedings of the Collo-
quium on Global Aspects of Coral Reefs: Heath, Hazards and History. pp 298–303
Holmes KE, Edinger EN, Hariyadi H, Limmon GV, Risk MJ (2000) Bioerosion of live massive corals and
branching coral rubble on Indonesian coral reefs. Mar Pollut Bull 40:606–617
Horiguchi T (2006) Masculinization of female gastropod mollusks induced by organotin compounds,
focusing on mechanism of actions of tributyltin and triphenyltin for development of imposex. Environ
Sci 13:77–87
Hunte W, Wittenberg M (1992) Effects of eutrophication and sedimentation on juvenile corals. Mar Biol
114:625–631
ICCS (2009) 18th International Coastal Cleanup, Singapore, September 2009. Consolidated Results: Man-
groves. http://coastalcleanup.nus.edu.sg/results/2009/M_OVERALL.htm. Last accessed Dec 17th 2009
Ismail A, Ramli R (1997) Trace metals in sediments and molluscs from an estuary receiving pig farms
effluent. Environ Technol 18:509–515
Isobe T, Takada H, Kanni M, Tsutsumi S, Isobe KO, Boonyatumanond R, Zakaria MP (2007) Distribution
of polycyclic aromatic hydrocarbons (PAHs) and phenolic endocrine disrupting chemicals in South and
Southeast Asian mussels. Environ Mon Assess 135:423–440
Iwata H, Tanabe S, Sakai N, Nishimura A, Tatsukawa R (1994) Geographical distribution of persistent
organochlorines in air, water and sediments from Asia and Oceania, and their implications for global
redistribution from lower latitudes. Environ Pollut 85:15–33
Jones MM (1995) Fishing debris in the Australian marine environment. Mar Pollut Bull 30:25–33
Jones RJ, Steven AL (1997) Effects of cyanide on corals in relation to cyanide fishing on reefs. Mar Freshw
Res 48:517–522
Jones RJ, Kildea T, Hoegh-guldberg O (1999) PAM chlorophyll fluorometry: a new in situ technique for
stress assessment in scleractinian corals, used to examine the effects of cyanide from cyanide fishing.
Mar Pollut Bull 38:864–874
Jørgensen BB, Richardson K (1996) Eutrophication in coastal marine ecosystem. American Geophysical
Union, Washington, DC
Kan-atireklap S, Tanabe S, Sanguansin J, Tabucanon MS, Hungspreugs M (1997) Contamination by butyltin
compounds and organochlorine residues in green mussel (Perna viridis. L.) from Thailand coastal
waters. Environ Poll 97:79–89

123
Biodivers Conserv (2010) 19:1063–1082 1079

Kannan N, Tanabe S, Ono M, Tatsukawa R (1989) Critical evaluation of polychlorinated biphenyl toxicity
in terrestrial and marine mammals: increasing impact of non-ortho and mono-ortho coplanar poly-
chlorinated biphenyls from land to ocean. Arch Environ Contam Toxicol 18:850–857
Kannan K, Tanabe S, Iwata H, Tatsukawa R (1995) Butyltins in muscle and liver of fish collected from
certain Asian and Oceanian countries. Environ Poll 90:279–290
Kawaguti S, Sakumoto D (1948) The effect of light on the calcium deposition of corals. Bull Oceanogr Inst
Taiwan 4:65–70
Kenchington R (1985) Coral reef ecosystems: a sustainable resource. Nature Resour 2:18–27
Kennish MJ (1997) Pollution impacts on marine biotic communities. CRC Marine Science Series
Kirk JTO (1977) Attentuation of light in natural waters. Aust J Mar Freshw Res 28:497–508
Laist D (1997) Impacts of marine debris: entanglement of marine life in marine debris including a com-
prehensive list of species with entanglement and ingestion records. In: Coe JM, Rogers DB (eds)
Marine debris: sources, impacts and solutions. Springer, New York, pp 99–139
Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in
Jamaica and Southeast Florida. Limnol Oceanogr 42:1119–1131
Lee DI, Cho HS, Jeong SB (2006) Distribution characteristics of marine litter on the sea bed of the East
China Sea and the South Sea of Korea. Estuar Coast Shelf 18:357–367
Liang Y, Tse MF, Young L, Wong MH (2007) Distribution patterns of polycyclic aromatic hydrocarbons
(PAHs) in the sediments and fish at Mai Po Marshes Nature Reserve, Hong Kong. Water Res 41:
1303–1311
Low JKY, Chou LM (1994) Sedimentation rates in Singapore waters. Proceedings of the Third ASEAN-
Australian Symposium on Living Coral Resources 2:697–701
Lu J (2003) Marine oil spill detection, statistics and mapping with ERS SAR imagery in South-east Asia. Int
J Remote Sens 24:3013–3032
Macan-Markar M (2007) Toxic backlash to Thai-Japan FTA. In: Asia Times. Asia Times Online (Holdings),
Ltd
Maria EJS, Siringan FP, Bulos AD, Sombrito EZ (2009) Estimating sediment accumulation rates in Manila
Bay, a marine pollution hot spot in the Seas of East Asia. Mar Pollut Bull 59:164–174
McManus JW (1997) Tropical marine fsheries and the future of coral reefs: a brief review with emphasis on
Southeast Asia. Coral Reefs 16:121–127
McManus JW, Reyes RBJ, Nanola CJ (1997) Effects of some destructive fishing methods on coral cover and
potential rates of recovery. Environ Manag 21:69–78
Menasveta P, Cheevaparanapiwat V (1981) Heavy metals, organochlorine pesticides and PCBs in green
mussels, mullets and sediments of river mouths in Thailand. Mar Pollut Bull 12:19–25
Mirza FB, Gray JS (1981) The fauna of benthic sediments from the organically enriched Oslofjord. Norway
J Exp Mar Biol Ecol 54:181–207
Monirith I, Ueno D, Takahashi S, Nakata H, Sudaryanto A, Subramanian A, Karuppiah S, Ismail A, Muchtar
M, Zheng J, Richardson BJ, Prudente M, Hue ND, Tana TS, Tkalin AV, Tanabe S (2003) Asia-Pacific
mussel watch: monitoring contamination of persistent organochlorine compounds in coastal waters of
Asian countries. Mar Pollut Bull 46:281–300
Moore CJ (2008) Synthetic polymers in the marine environment: a rapidly increasing, long-term threat.
Environ Res 108:131–139
Moser ML, Lee DS (1992) A fourteen-year survey of plastic ingestion by Western North Atlantic seabirds.
Colon Waterbird 15:83–94
Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature
450:98–101
National Research Council (1979) Polychlorinated biphenyls. National Academy of Sciences, Washington
DC, pp 25–28
Negri AP, Heyward AJ (2001) Inhibition of coral fertilisation and larval metamorphosis by tributyltin and
copper. Mar Environ Res 51:17–27
Neira C, Rackemann M (1996) Black spots produced by buried macroalgae in intertidal sandy sediments of
the Wadden Sea: effects on the meiobenthos. J Sea Res 36:153–170
Ng KL, Obbard JP (2006) Prevalence of microplastics in Singapore’s coastal marine environment. Mar
Pollut Bull 52:761–767
Olsgard F, Hasle JR (1993) Impact of waste from titanium mining on benthic fauna. J Exp Mar Biol Ecol
172:185–213
Onitsuka T, Kawamura T, Ohashi S, Iwanaga S, Horii T, Watanabe Y (2008) Effects of sediments on larval
settlement of abalone Haliotis diversicolor. J Exp Mar Biol Ecol 365:53–58
Paerl HW, Dennis RL, Whitall DR (2002) Atmospheric deposition of nitrogen: implications for nutrient
over-enrichment of coastal waters. Estuaries 25:677–693

123
1080 Biodivers Conserv (2010) 19:1063–1082

PCD (no date) Thailand state of environment: the decade of 1990s. Pollution Control Department (PCD),
Bangkok
Portmann JE (1975) The bioaccumulation and effects of organochlorine pesticides in marine animals. Proc
R Soc Lond B 189:291–304
Pruter AT (1987) Sources, quantities and distribution of persistent plastics in the marine environment. Mar
Pollut Bull 18:305–310
Purcell JE, Uye S-I, Lo W-T (2007) Anthropogenic causes of jellyfish blooms and their direct consequences
for humans: a review. Mar Ecol Prog Ser 350:153–174
Ramachandran S, Patel TR, Colbo MH (1997) Effect of copper and cadmium on three Malaysian tropical
estuarine invertebrate larvae. Ecotox Environ Safe 36:183–188
Reichelt-Brushett AJ, Harrison PL (1999) The effect of copper, zinc and cadmium on fertilization success of
gametes from scleractinian reef corals. Mar Pollut Bull 38:182–187
Reichelt-Brushett AJ, Harrison PL (2000) The effect of copper on the settlement success of larvae from the
scleractinian coral Acropora tenuis. Mar Pollut Bull 41:385–391
Riegl B (1995) Effects of sand deposition on scleractinian and alcyonacean corals. Mar Biol 121:517–526
Riegl B, Branch GM (1995) Effects of sediment on the energy budgets of four scleractinian (Bourne 1900)
and five alcyonacean (Lamouroux 1816) corals. J Exp Mar Biol Ecol 186:259–275
Riegl B, Heine C, Branch GM (1996) Function of funnel-shaped coral growth in a high-sedimentation
environment. Mar Ecol Prog Ser 145:87–93
Ritter L, Solomon KR, Forget J (1997) Persistent organic pollutants. An assessment report on: DDT-aldrin-
dieldrin-endrin-chlordane, heptachlor-hexachlorobenzene, mirex-toxaphene, polychlorinated biphe-
nyls, dioxins and furans. The International Programme on Chemical Safety (IPCS) within the
framework of the Inter-Organization Programme for the Sound Management of Chemicals (IOMC)
Rogers CS (1983) Sublethal and lethal effects of sediments applied to common Caribbean Reef corals in the
field. Mar Pollut Bull 14:378–382
Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:
185–202
Ross PS, Ellis GM, Ikonomou MG, Barrett-Lennard LG, Addison RF (2000) High PCB concentrations in
free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference. Mar Pollut
Bull 40:504–515
Saiz-Salinas JI, Urkiaga-Alberdi J (1999) Faunal responses to turbidity in a man-modified bay (Bilbao,
Spain). Mar Environ Res 47:331–347
San Diego-McGlone ML, Azanza RV, Villanoy CL, Jacinto GS (2008) Eutrophic waters, algal bloom and
fish kill in fish farming areas in Bolinao, Pangasinan, Philippines. Mar Pollut Bull 57:295–301
Shazili NAM, Yunus K, Ahmad AS, Abdullah N, Rashid MKA (2006) Heavy metal pollution status in the
Malaysian aquatic environment. Aquat Ecosyst Health 9:137–145
Siegert F, Hoffmann AA (2000) The 1998 forest fires in East Kalimantan (Indonesia): A quantitative
evaluation using high resolution, multitemporal ERS-2 SAR Images and NOAA-AVHRR Hotspot
Data. Remote Sens Environ 72:64–77
Sien CL, Kirkman H (2000) Overview on Land-based sources and activities affecting the marine envi-
ronment in the East Asian Seas. UNEP Regional Seas Reports and Studies 173
Song Y-H (2008) The potential marine pollution threat from oil and gas development activities in the
disputed South China Sea/Spratly Area: a role that Taiwan can play. Ocean Dev Int Law 39:150–177
Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. UNEP-WCMC and the University of
California Press, Berkley
Stafford-Smith MG (1992) Mortality of the hard coral Leptoria phrygia under persistent sediment influx.
Proc 7th Int Coral Reef Symp 1:289–299
Stafford-Smith MG (1993) Sediment rejection effeciency of 22 species of Australian scleractinian corals.
Mar Biol 115:229–243
Stafford-Smith MG, Ormond RFG (1992) Sediment rejection mechanisms of 42 species of Australian
scleractinian corals. Aust J Mar Fresh Res 43:683–705
Stern GA, Halsall CJ, Barrie LA, Muir DCG, Fellin P, Rosenberg B, Rovinsk FY, Kononov EY, Pastuhov B
(1997) Polychlorinated Biphenyls in Arctic Air. 1. Temporal and spatial trends: 1992–1994. Environ
Sci Technol 31:3619–3628
Stott P (1988) The Forest as phoenix: towards a biogeography of fire in mainland South East Asia. Geogr J
154:337–350
Sujitno S (1977) Some notes on offshore exploration for tin in Indonesia. United Nations ESCAP, CCOP
Tech Bull 11:169–181
Swennen C, Sampantarak U, Ruttanadakul N (2009) TBT-pollution in the Gulf of Thailand: a re-inspection
of imposex incidence after 10 years. Mar Pollut Bull 58:526–532

123
Biodivers Conserv (2010) 19:1063–1082 1081

Takahashi S, Mukai H, Tanabe S, Sakayama K, Miyazaki T, Masuno H (1999) Butyltin residues in livers of
humans and wild terrestrial mammals and in plastic products. Environ Pollut 106:213–218
Tan AK-J (2004) Environmental laws and institutions in Southeast Asia: a review of recent developments.
Singapore Yearbook Int Law 8:177–192
Tanabe S (1985) Distribution, behaviour and fate of PCBs in the marine environment. J Oceanogr Soc Jpn
41:358–370
Tanabe S (1988) PCB problems in the future: foresight from current knowledge. Environ Pollut 50:5–28
Taylor D (2010) Biomass burning, humans and climate change in Southeast Asia. Biodivers Conserv. doi:
10.1007/s10531-009-9756-6 (this special issue)
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
Tun K, Chou LM, Cabanban A, Tuan VS, Philreefs, Yeemin T, Suharsono, Sour K, Lane D (2004) Status of
coral reefs, coral reef monitoring and management in Southeast Asia, 2004. In: Wilkinson C (ed) Status
of coral reefs of the world: 2004, vol 1. Australian Institute of Marine Science, Townsville,
Queensland, Australia, p 301
Turk TR, Risk MJ (1981) Effects of sedimentation on infaunal invertebrate populations of Cobequid Bay,
Bay of Fundy. Can J Fish Aquat Sci 38:642–648
UNEP (2002) Regionally based assessment of persistent toxic substances. South East Asia and South
Pacific, Regional Report
UNEP (2005) Marine Litter, an analytical overview
UNEP EAS/RCU (2008) Marine litter in the East Asian Seas Region
UNEP (2009) Marine litter: a global challenge
UNEP/GPA (2006) The state of the marine environment: trends and processes
Uneputty PA, Evans SM (1997a) Accumulation of beach litter on islands of the Pulau Seribu Archipelago,
Indonesia. Mar Pollut Bull 34:652–655
Uneputty PA, Evans SM (1997b) The impact of plastic debris on the biota of tidal flats in Ambon Bay
(Eastern Indonesia). Mar Environ Res 44:233–242
USDA (2009) Export/import statistics for bulk, intermediate, and consumer oriented (BICO) foods and
beverages
van der Meij SET, Moolenbeek RG, Hoeksema BW (2009) Decline of the Jakarta Bay molluscan fauna
linked to human impact. Mar Pollut Bull 59:101–107
Varanasi U, Stein JE, Nishimoto M (1989) Biotransformation and disposition of polycyclic aromatic
hydrocarbons (PAH) in fish. In: Varanasi U (ed) Metabolism of polycyclic aromatic hydrocarbons in
the aquatic environment. CRC, Boca Raton, FL, pp 93–150
Viberg H, Fredriksson A, Eriksson P (2002) Neonatal exposure to the brominated flame retardant 2, 20 , 4, 40 ,
5-pentabromodiphenyl ether causes altered susceptibility in the cholinergic transmitter system in the
adult mouse. Toxicol Sci 67:104–107
Villanueva RD, Yap HT, Montaño NE (2005) Survivorship of coral juveniles in a fish farm environment.
Mar Pollut Bull 51:580–589
Villanueva RD, Yap HT, Montaño NE (2006) Intensive fish farming in the Philippines is detrimental to the
reef-building coral Pocillopora damicornis. Mar Ecol Prog Ser 310:165–174
Walker DI, Ormond RFG (1982) Coral death from sewage and phosphate pollution at Aqaba, Red Sea. Mar
Pollut Bull 13:21–25
Warren-Rhodes K, Sadovy Y, Cesar H (2003) Marine ecosystem appropriation in the Indo-Pacific: a case
study of the live reef fish food trade. Ambio 32:481–488
Weiffen M, Moller M, Mauck B, Dehnhardt G (2006) Effect of water turbidity on the visual acuity of harbor
seals (Phoca vitulina). Vis Res 46:1777–1783
Willoughby NG (1986) Man-made litter on the shore of the Thousand Island Archipelago, Java. Mar Pollut
Bull 17:224–228
Willoughby NG, Sangkoyo H, Lakaseru BO (1997) Beach litter: an increasing and changing problem for
Indonesia. Mar Pollut Bull 34:469–478
Wolff MS, Toniolo PG, Lee EW, Rivera M, Dubin N (1993) Blood levels of organochlorine residues and
risk of breast cancer. J Natl Cancer Inst 85:648–652
Wu RSS (1995) The environmental impact of marine fish culture: towards a sustainable future. Mar Pollut
Bull 31:159–166
Wurl O, Obbard JP (2005) Organochlorine pesticides, polychlorinated biphenyls and polybrominated
diphenyl ethers in Singapore’s coastal marine sediments. Chemosphere 58:925–933
Yang G-P, Liu X-L, Zhang J-W (1998) Distribution of dibenzothiophene in the sediments of the South
China Sea. Environ Poll 101:405–414
Yap LG, Azanza RV, Talaue-McManus L (2004) The community composition and production of phyto-
plankton in fish pens of Cape Bolinao, Pangasinan: a field study. Mar Pollut Bull 49:819–832

123
1082 Biodivers Conserv (2010) 19:1063–1082

Zakaria MP, Takada H, Tsutsumi S, Ohno K, Yamada J, Kouno E, Kumata H (2002) Distribution of
polycyclic aromatic hydrocarbons (PAHs) in rivers and estuaries in Malaysia: a widespread input of
petrogenic PAHs. Env Sci Tech 36:1907–1918
Zhou T, Taylor MM, DeVito MJ, Crofton KM (2002) Developmental exposure to brominated diphenyl
ethers results in thyroid hormone disruption. Toxicol Sci 66:105–116

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