6 PH

Vol.
15 July 2015 Volume 15 July 2015

Print ISSN 2244-1573 Online ISSN 2244-1581
International Peer Reviewed Journal
doi: http://dx.doi.org/10.7718/ijec.v15i1.999
Journal Metrics: H Index = 1 from Publish or Perish
This journal is included in Thomson Reuters Journal Masterlist
Published by IAMURE Multidisciplinary Research,
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Nutrient Enrichment, Sedimentation,

Heavy Metals and Plastic Pollution
in the Marine Environment and its
Implications on Philippine Marine
Biodiversity: A Review
NEIL ANGELO S. ABREO
http://orcid.org/0000-0003-3562-0309
nas.abreo@gmail.com
Davao Medical School Foundation, Inc.
Davao City, Philippines
EDISON D. MACUSI
http://orcid.org/0000-0002-9714-1074
edmacusi@gmail.com
Aquaculture and Fisheries Group, Wageningen Institute of Animal Sciences,
Wageningen University of Life, Wageningen, The Netherlands
GINALYN C. CUENCA
http://orcid.org/0000-0003-0261-5271
djinaleene8@gmail.com
111
IAMURE International Journal of Ecology and Conservation
CYRIL TOM B. RANARA

http://orcid.org/0000-0002-3260-9289
tomranara74@yahoo.com
Davao Del Norte State College
Panabo City, Philippines
MICHAEL B. ANDAM
http://orcid.org/0000-0003-0552-6055
michael_andam@ymail.com
LEMUEL C. CARDONA
http://orcid.org/ 0000-0001-7981-6202
cardona_lemuel@yahoo.com
GLIO FLORGILEY P. ARABEJO

http://orcid.org/orcid.org/0000-0003-1917-3895
Gunning Fog Index: 10.15 Originality: 100% Grammar Check: 90%

Flesch Reading Ease: 49.97 Plagiarism:0%
ABSTRACT
Marine biodiversity plays a vital role in ecosystem resilience and stability

against climate change and alien species invasions, among others. This also plays
a role in the provision of ecosystem services and functions that benefits humans.
However due to anthropogenic activities and population increase, marine
biodiversity have been affected most. We conducted a review using open-sourced
journals on the effects of nutrient enrichment, sedimentation, heavy metals and
plastic pollution in the marine environment and its implications on marine
biodiversity. Lethal and sub-lethal effects were observed in different organisms
that could affect marine biodiversity directly or indirectly. Direct effects include
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Volume 15 July 2015
mortality of organisms while indirect effects include habitat degradation or

alteration, a simplified food web, increase alien species invasion and reduced
fitness of organisms. Human land use change, coastal construction activities,
untreated sewage discharges, pesticides, mine tailings, uncollected, unsegregated
and improperly dumped garbages and unabated garbage dumping at sea have
been found to negatively influence marine biodiversity. In the Philippines, very
few studies have been conducted with regards to marine pollution, especially
on marine plastic debris, and even fewer studies have been made that tackles
the effect of these stressors at an ecosystem level. Furthermore, this review has
identified direct and indirect effects of pollution stressors on marine organisms
which include: mortality and reduced fitness, vulnerability to disease or sickness,-
habitat degradation, and food web simplification.
KEYWORDS
Ecology, nutrient enrichment, sedimentation, plastic, biodiversity, literature

review, pollution, Philippines
INTRODUCTION
Biodiversity promotes community stability and productivity of an ecosystem

(Corcoran & Boeing, 2012). An ecosystem that has high biodiversity is found to
be more resilient to the effects of climate change and is less susceptible to invasions
of alien species (Hughes et al., 2003; Downing et al., 2012). A more diverse
ecosystem also provides more benefits to the human population compared to a
less diverse one (Larsen Turner, & Brooks, 2012).The direct and indirect benefits
that humans get from ecosystems, called ecosystem services and functions, are
affected by biodiversity (Worm et al., 2006). Sadly, there is an observed trend of
global biodiversity decline. Although there are efforts in countering this decline,
such as establishment of protected areas (Christie, White, & Deguit 2002; Weeks
et al., 2010), the decline still continues (Mora & Sale, 2011).
Human activities can have a direct or indirect effect that leads to biodiversity
decline (Hughes et al., 2003; Parravicini et al., 2013; Sheehan et al., 2013). In
the marine environment, for example, the increase in human settlement has been
observed to have also increased the influx of sediments to the Great Barrier Reef
(McCulloch et al., 2003) and areas of high human population has been shown
to host very high pollutants (Gregory, 1978; Derraik, 2002; Reisser et al., 2013).
113
Moreover, coral reef ecosystems were observed to be less stable near heavily
populated islands (Weijerman, Fulton, & Parrish, 2013). Organisms residing
in marine environments near human populated areas were found contaminated
with pollutants such as heavy metals and polybromenated diphenylethers
(PBDEs) and suffers from diseases and growth anomalies (Aeby et al., 2011;
Kennedy, Twilley, Kleypas, Cowan Jr, & Har,e 2002; Komoroske, Lewison,
Seminoff, Deheyn, & Dutton, 2011). Lotze et al., (2006) showed that human
impacts caused depletion of more than 90% of important species, destruction of
more than 65% of seagrass and wetland habitats, degradation of water quality
and acceleration of the introduction of non-native species. According to Myers,
Mittermeier, Mittermeier, Da Fonseca, and Kent (2000), biodiversity hotspots
are mostly in developing countries with large populations. The rapid economic
rise in developing countries has also been coupled by rapid increase in marine
pollution (Lebreton, Greer, & Borrero, 2012; van Sebille, England, & Froyland,
2012).
One cause of biodiversity decline is land-based pollution defined as pollution
of maritime zones caused by discharges from coastal establishments and other
sources situated on land or artificial structures (UNITAR, 2014). Several studies
have shown the connection of land and marine pollution ( Woolger, 2009; Okuku
et al., 2011; Li et al., 2012). Human activities on land such as tourism, trampling,
farming, garbage dumping, logging and coastal construction activities from
jetties to ports have been found to have negative effects on marine organisms and
marine ecosystems (Fabricius, 2005; Deepananda & Macusi, 2012; Parravicini
et al., 2013). Human land use, for example, has caused the decline of benthic
marine organism diversity (Takarina & Adiwibowo, 2011; Deepananda &
Macusi, 2013). The increase in coastal development and discharge of untreated
waste into rivers and near-shore waters has become a major threat to marine
biodiversity. These have increased sedimentation, nutrient enrichment, biological
pollutants and marine debris in marine ecosystems ( Fabricius, 2005; Bullock,
Kretsch, & Candon, 2008; Smith & Edgar, 2014;). Marine debris and nutrient
enrichment have caused numerous mortality to marine organisms (Villanueva,
Yap, & Montao, 2005; Lazar & Graan, 2011; Di Beneditto & Ramos, 2014;
Lavers, Bond, & Hutton, 2014), while heavy metals have also resulted to declines
of diversity of fouling assemblages (Canning-Clode,Fofonoff, Riedel, Torchin, &
Ruiz, 2011).
With the increasing trend of human population, marine pollution is also
increasing. Commonly, studies on marine pollution have tackled the individual
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effects of different pollutants to marine organisms and the marine environment.

There are minimal studies on synergistic effects of these pollutants and does not
provide a holistic view of the pollution problem. Currently, there is a dearth of
literature on effects of marine pollutants on Philippine marine biodiversity. Thus,
this review focused on the effects of sedimentation and nutrient enrichment, heavy
metals and plastic pollution. This paper will review the direct and indirect impacts
of habitat degradation as a result of pollution stressors such as sedimentation,
nutrient enrichment, heavy metals and plastic debris on biodiversity of marine
organisms. At present, there is a dearth of information on the effects of these
stressors to marine organisms and marine biodiversity, in general.
OBJECTIVES OF THE STUDY
This review discussed the implications of sedimentation, nutrient enrichment,

heavy metal and plastic pollution on the mortality of marine organisms and
damage to marine ecosystems.
METHODOLOGY
This study used literature that deal with marine pollution and its impacts on
marine biodiversity in the Philippines. Literature search was conducted using
information sources such as open access journals (DOAJ), Google Scholar,
Philippine e-Journals, Research Gate and Mendeley. Search phrases used include:
marine pollution, sedimentation, siltation, eutrophication, nutrient enrichment,
plastic ingestion and heavy metals. Both published and gray literature was
utilized to compensate for the limited published articles focused on marine
pollution in the Philippines. A thematic discussion on sedimentation and nutrient
enrichment, heavy metals and plastic pollution on marine organisms and marine
habitats along with its implications on marine biodiversity are presented in this
paper.
RESULTS AND DISCUSSION
Sedimentation and nutrient enrichment

One of the leading cause of marine biodiversity decline is habitat damage
or habitat loss that leads to the extinction of species (Pimm & Raven, 2000).
Generally, habitat loss or even loss of habitat structure can lead to lower
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biomasses and decline in species richness (Airoldi, Balata, & Beck, 2008;
Pratchett, Hoey, Wilson, Messmer, & Graham 2011). Sedimentation and
nutrient enrichment has been found to have damaging effects to corals and
seagrasses, which provides habitats a number of marine organisms (ISRS, 2004;
Mnard, Turgeon, Roche, Binning, & Kramer, 2012) or directly cause mortality
to marine organisms (Airoldi & Cinelli, 1997; Hutchinson & Williams, 2003,
Macusi & Deepananda, 2013) Eutrophication can be defined as the increase of
organic carbon in an ecosystem (Nixon, 1995). It is the result of a combination
of factors that leads to an increase in the growth of primary producers in aquatic
and marine environments (Schindler, 2006). The growth of primary producers
is due to increasing availability or levels of limiting factors, particularly nutrients
(Correll, 1998). One characteristic of a eutrophic body of water is the presence of
high densities of algae that utilizes excess nutrients (Carpenter et al., 1998). This
process is a natural phenomenon that occurs over centuries in lakes and shallow
marine environments as more sediments are deposited in these bodies of water
(Chislock et al.,2013). Cultural eutrophication, however, is the acceleration of
eutrophication due to anthropogenic activities and observed to have adverse
effects of the environment (Smith & Schindler, 2009; Chrislock et al., 2013).
Sedimentation plays a role in eutrophication by providing additional nutrients,
such as phosphorous and nitrogen, to bodies of water. Nutrients attach to the
sediments from agricultural lands, that aids in its transport to bodies of water
through surface runoffs and erosion that disrupts normal ecosystem functioning
(Fabricius, 2005; Erhunmwunse, Dirisu, & Ogbeibu, 2013).
The synergistic effect of sedimentation and nutrient enrichment that
negatively affect marine biodiversity includes: (1) promotion of algal blooms
which affects marine organisms by clogging or lacerating breathing organs,
produce potent toxins (San Diego-McGlone et al., 2008; Craig, 2012), cause
hypoxic environment due to the oxygen usage of decomposers in decomposing
algae die-offs (Farrell, Tupas, & Murawski, 2010) that may also result to habitat
compression (Prince & Goodyear, 2006); (2) blocking of sunlight that prevents
other marine plants and corals from accessing light for photosynthesis (Kumara,
2013); (3) burial and smothering of marine organisms (Cabaco, Santos, &
Duarte 2008 ); and (4) promotion of environmental parameters that may favour
competitors of ecosystem engineers or favours dominance of a single species that
reduces habitat heterogeneity (Villanueva et al., 2005; 2006; Powell et al., 2014).
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Effects of sedimentation and nutrient enrichment on corals

Adult and juvenile corals are known to be susceptible to increase in sediments
and nutrients in marine environments. In a review by Bartley (2014), maximum
sedimentation rate should be at 15 mg cm-2 d-1 and average suspended sediment
concentration should be at 2.4 mg L-1 to avert coral mortality. This is supported
by the experiment conducted by Villanueva et al., (2005) in Bolinao Pangasinan,
where total mortality of coral nubbins were observed in sites where sedimentation
(193 g m-2 d-1) and total suspended solids (~7.2mg L -1) was high. Possible causes
of mortality of these corals as stated by Villanueva et al., (2005) are: (1) Increase
in nutrients have increased the growth of competitors of coral juveniles thus
outcompeting coral juveniles; (2) increase in nutrients lowers the dissolved
oxygen levels; (3) increased sedimentation increases the turbidity and thus,
lessens the amount of light that can be utilized by the zooxanthellae associated
with the coral juveniles, leading to lesser nutrition for the coral juveniles and (4)
increased sedimentation smothers and buries the coral juveniles which is known
to be the major cause of higher mortality and lower abundance of juvenile corals
in eutrophic reefs. While Johnson et al. (2010) have identified that increase
in nutrient (e.g. Nitrogen and Phosphorous) loading can change host/vector
density, distribution, resistance, pathogen virulence, or direct supplementation
of pathogens. Diseases in corals such as the Black Band Disease (BBD) has been
observed to have a direct relationship with increasing nitrite concentrations. The
average nitrite concentration of study sites with BBD was significantly higher
(0.19 M) as compared to 0.14 M of sites without BBD (Kuta & Richardson,
2002). Results of an experiment conducted by Bruno et al., (2003) suggest that
nutrient enrichment may play a role in the increase of coral disease severity since
additional nutrients are utilized by marine pathogens, that in turn, increase the
virulence and fitness of the pathogenic organisms. In the experiment, disease
advancement and tissue loss was observed at 0.3-0.5cm month-1, an average
rate 1.8 times compared to the control set up, when corals were subjected to
treatments with concentration ranges of 1.0 to 6.4 M nitrate, 0.9 to 4.6 M
phosphorous and 1.0 to 11.0 M ammonium. Increase in sedimentation have
also been observed by Wesseling, Uychiaoco, Alio, and Vermaat (2001) to
increase partial necrosis in Porites corals and decrease in coral cover. This result
was in conjunction to the study conducted by Haapkyl et al. (2011) where they
have also suggested, that aside from increased in virulence of pathogens, coral
immunity could have been lowered by the increase in stress the coral experienced,
possibly from sedimentation (Junjie, Browne, Erftemeijer, & Todd 2014).
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The increase in nutrients also encourages the growth of algae, that has
been observed by Sweet, Bythell and Nugues (2013) to be a reservoir for coral
pathogens. In the study, out of the five ciliates that were detected in algae, three
were found to be associated with coral reef diseases. In the same study, a number
of bacteria that were detected in algae were also known to be associated with
diseases in corals.
Larval settlement of different coral species is also negatively affected by
sedimentation (Babcock & Smith, 2000; Goh & Lee, 2008; Erftemeijer,
Hagedorn, Laterveer, Craggs, & Guest, 2012). Sediments cover hard substrates
making it loose and unstable which prevents the coral larvae from establishing
itself (Berry, Rubinstein, Melzian, & Hill, 2003). Moreover, corals spend energy
for removal of sediments (Junjie et al., 2014) and, therefore, lesser energy is
allotted to fecundity leading to less coral reproduction (Kojis & Quinn, 1984).
Coral recovery was also observed to be slow when it is exposed to sediment-
induced stress (Goatley & Bellwood, 2013).
Effects of sedimentation and nutrient enrichment on seagrass

Seagrassses, which make up one of the most productive marine ecosystems
(Naser, 2002; Mvungi, 2011; Gillis et al., 2014;) and provides a myriad of
ecosystem services such as nursery for fishes and other marine organisms,
carbon sequestration, sediment stability and filtration of other pollutants and
heavy metals (Greiner, McGlathery, Gunnell, & McKee 2013; Ahmad, Azman,
Said, , & Sabri, 2014), and was found by Gillis et al. (2014) to be a significant
contributor of organic matter to other marine ecosystems. These habitat-forming
species, which provide a very productive ecosystem are also negatively impacted
by increased rate of sedimentation and eutrophication (Coll, Schmidt, Romanuk,
& Lotze, 2011). Effects of eutrophication and sedimentation on seagrass beds
include reduction of aboveground and belowground biomass, decrease shoot
density, or even total eradication, as an effect to the increase in the density and
abundance of phytoplankton, epiphytic and benthic algae (Hauxwell, Clelland,
Behr, & Valiela, 1998; Coll et al., 2011) or by burial (Cabaco et al., 2008).
Seagrasses have very high light requirements, they require more than 23%
incident radiation relative to other angiosperms (Orth et al., 2006), and the
increase in turbidity brought about by increased suspended solids and increase in
phytoplankton and macroalgae abundance in the water column can limit light
penetration and lessens the photosynthetic activities of seagrasses resulting to
lower nutrition for the plant. Shading has a more profound effect on seagrass
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recruitment as new seagrasses shoots were also found to be susceptible to limited

light (Hauxwell, Cebrin, & Valiela, 2003; Schmidt, Wysmyk, Craig, & Lotze,
2012; York et al., 2013). Seagrass blades also becomes substrates for epiphytic
algae and increase in the abundance of these algae due to increased levels of
limiting factors ,such as nutrients, cause mechanical stress to seagrasses (Howard
& Short, 1986). According to Hauxwell et al., (2001), macroalgae can also alter
biogeochemical conditions (e.g. Lowers redox conditions and potentially toxic
concentrations of NH4+) of the ecosystems that can potentially have a negative
effects to marine organisms.
A study conducted by Coll et al. (2011) showed that eutrophication altered
the trophic interactions in a seagrass community. As food webs in a seagrass
community were subjected to anthropogenic stress, they become more degraded,
simplified and is less robust and becomes more vulnerable to species extinction.
A study conducted by Hauxwell et al. (1998) showed that there was a decline
on herbivore abundance as nitrogen load increased even though there was an
increase in macroalgal abundance. Loss of herbivores in seagrass ecosystems
(possibly due to anoxic conditions in eutrophic environment) could have ripple
effects as these herbivores serve as links, where energy of primary producers are
able to reach higher consumers (Heck & Valentine, 2006).
Effects of habitat loss or alteration on marine biodiversity

The effects of sedimentation and nutrient enrichment to reef-building coral
species and seagrasses also affect other marine organisms that occupy the habitats
that these organisms provide (Mnard et al., 2012). The amount of shelter that
these organisms provide affects the number of individuals and species (Rogers
1990). Loss in live coral cover, for example, has led to a net decline of coral reef
fish diversity. It was suggested that 75% of coral reef fishes rely on live corals
for survival (Jones et al., 2004) and according to a review by Pratchett et al.
(2011) a coral loss of >60% affects reef fish diversity negatively. Changes in
species composition as a result of sedimentation and nutrient enrichment has
been observed. A study conducted by Powell et al., (2014) has shown that a coral
reef exposed to sedimentation changed to a low diversity, sponge-dominated
reefs which affected the ecosystem services that it provides. Sponge species were
observed to dominate in coral reef areas where there are high sedimentation and
low coral diversity. Coral reefs exposed to high sedimentation (36 mg cm-2 d-1)
event in China were also found to have suffered mean live coral cover decline
from 30.5% to 9% and underwent a shift in the dominant coral species to a more
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sedimentation tolerant species (Li et. al., 2013). Seagrass beds were also observed
to follow a same pattern when exposed to sedimentation. Different species of
seagrass react differently to sedimentation. Thus, allowing for dominance of a
particular species and resulting to changes in species composition (Cabaco et al.,
2008). Changes in the community structure also entail changes in marine fauna
in those habitats and could promote the displacement of resident reef-associated
species. A study by Ray et al., (2014) showed that a change in seagrass composition
also exhibited a change in the fauna of seagrass beds. In the study, three different
seagrass species exhibited >50% dissimilarity on faunal composition, suggesting
that there is a species-specific relationship among several different characteristics
of the seagrass community. Box, Martin, and Deudero (2010) also observed a
change in associated polychaete assemblage as a Posidonia oceanic bed is being
replaced by an invasive macroalgae, Caulerpa racemosa. Although there was no
significant difference in diversity, results showed that there was a change in the
dominant species of ploychaetes associated with C. racemosa that may influence
trophic interactions.
Moreover, degradation of one marine ecosystem has implications on other
marine ecosystems. Study on habitat use of fishes by Honda, Nakamura, Nakaoka,
Uy, and Fortes (2013) showed fishes use multiple habitats to complete their life
cycle. The absence of one type of ecosystem can have adverse effects on fish
populations. Seagrass ecosystems, for example, has been observed to be a source
of carbon for other marine ecosystems. The products of seagrass beds were found
to be exported to other marine ecosystems (Gillis et al., 2014). Seagrasses help
maintain coral reef systems by lessening sedimentation by altering/slowing water
movement. Thus, promoting the settlement of suspended particles, and other
pollutants, such as heavy metals through bioaccumulation (Madsen, Chambers,
James, Koch, & Westlake, 2001; Thangaradjou, Nobi, Dilipan, Sivakumar, &
Susila, 2010; Ondiviela et al., 2014; Ahmad et al., 2014).
Heavy metals in the marine environment and its effects on marine organisms
The term heavy metal is defined in many ways and is often misleading
(Duffus, 2002; Hodson, 2004). A good discussion on the definition of the term
heavy metal with reference to life sciences is provided by Appenroth (2010)
and Nagajyoti, Lee and Sreekanth (2010). In general, these metals: zinc (Zn),
cadmium (Cd), copper (Cu), mercury (Hg), chromium (Cr), lead (Pb), arsenic
(As), cobalt (Co), nickel (Ni), manganese (Mn), Selenium (Se), Silver (Ag),
Cesium (Cs), Aluminum (Al), Strontium (Sr), Molybdenum (Mo), Uranium
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(U) and iron (Fe) are termed as heavy metals because of their toxicity to living
organisms (Singh, Gautam, Mishra, & Gupta, 2011).
Heavy metals in the marine environment have become one of the problems
that have arisen from land-based pollution and is faced by different countries
worldwide. Heavy metals accumulate in sediment and water of marine
environment (Irnawati, Susanto, & Syabana, 2014). This is a problem since
heavy metals are very persistent in the environment (David, 2002). Heavy metals
have an effect on living organisms even when their natural concentration are very
low (Khayatzayadeh & Abbasi, 2010; Jakimska, Konieczka, Skra, & Namiesnik,
2011) and increasing their concentration through anthropogenic activities could
spell disaster for certain living organisms (Ramakritinan, Chandurvelan &
Kumaragu, 2012). Heavy metal pollution has been observed to have negative
effects on marine organisms and pose a health risk to humans. A review conducted
by Govind and Madhuri (2014) has shown the specific effects of different heavy
metals to the environment and human health.
Table 1. Presence of heavy metals in different marine and freshwater organisms.

Species Heavy metals References
Mangrove
Avicennia marina Pb, Cu, Cr Al Anouti, 2014
Seagrass
Enhalus acoroides Mn, Al, Fe, Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Halophila ovalis Mn, Al, Fe, Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Halophila ovata Mn, Al, Fe, Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Thalassia hemprichii Mn, Al, Fe Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Cymodocea rotundata Mn, Al, Fe Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Halodule uninervis Mn, Al, Fe Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Halodule pinifolia Mn, Al, Fe Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Syngridium isoetifolium Mn, Al, Fe Cr, Cu, Zn,Pb, Cd, Ni, Co Thangaradjou et al., 2010
Joksimovic & Stankovics,
Posidonia oceanic Co, Ni, As, Cd, Hg, Pb
2012
Invertebrates
Joksimovic & Stankovics,
2012 ; Bogdanovi
Mytilus galloprovincialis Co, Ni, As, Cd, Hg, Pb, Cr, Cu, V
et al., 2014; Spada
&Annicchiarico, 2013
Perna viridis Zn, Pb, Cr, Co, Cu, Cd, Ni Kumar & Achyutan 2007
Ostrea edulis Co, Ni, As, Cd, Hg, Pb Bogdanovic et al., 2014
121
Chlamis varia Co, Ni, As, Cd, Hg, Pb Bogdanovic et al., 2014
Venus verrucosa Co, Ni, As, Cd, Hg, Pb Bogdanovic et al., 2014
Paracentrotus lividus Zn, Pb, Cu, Cd, Fe Soualili et al., 2008
Cymbula nigra As, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn Guerra-Garca et al., 2010
Patella caerulea As, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn Guerra-Garcia et al., 2010
Caprella acanthifera As, Cr, Fe, Mn, Ni, Zn Guerra-Garcia et al., 2010
Caprella danilevskii Cr, Fe, Mn, Ni, Zn Guerra-Garcia et al., 2010
Caprella dilatata As, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn Guerra-Garcia et al., 2010
Caprella equilibra As, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn Guerra-Garcia et al., 2010
Caprella grandimana As, Cr, Cu, Fe, Mn, Ni, Zn Guerra-Garcia et al., 2010
Caprella hirsuta Fe, Mn, Zn Guerra-Garcia et al., 2010
Caprella liparotensis As, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn Guerra-Garcia et al., 2010
Caprella penantis As, Cr, Cu, Fe, Hg, Mn, Ni, Zn Guerra-Garcia et al., 2010
Solenocera crassicornis Zn, Cu, Co, Cr, Cd Kumar & Achyutan, 2007
Scylla serrate Pb, Zn, Co, Cu, Cd, Cr Kumar & Achyutan, 2007
Aristeusan tennatus Zn, Pb, Cd Ismahene and Hadi 2012
Parapenaeus longirostris Zn, Pb, Cd Ismahene and Hadi 2012
Palaemon serratus Zn, Pb, Cd Ismahene and Hadi 2012
Patella vulgate Zn, Cd, Pb, Cu Perez-Lopez et al., 2003
Vertebrates
Selaroides leptolepis Zn, Cu, Pb Kamaruzzaman et al., 2010
Euthynnus affinis Zn, Cu, Pb Kamaruzzaman et al., 2010
Parastromateus niger Zn, Cu, Pb Kamaruzzaman et al., 2010
Lutjanius malabaricus Zn, Cu, Pb Kamaruzzaman et al., 2010
Epinephelus sexfasciatus Zn, Cu, Pb Kamaruzzaman et al., 2010
Rastrelliger kanagurta Zn, Cu, Pb Kamaruzzaman et al., 2010
Nemipterus japonicus Zn, Cu, Pb Kamaruzzaman et al., 2010
Megalaspis cordyla Zn, Cu, Pb Kamaruzzaman et al., 2010
Carnyx hippos Zn, Cr, Pb, Cu, Ni, Co, Cd Kumar & Achyutan, 2007
Al, As, Cd, Cu, Pb, Mn, Hg, Se, Sr,
Chelonia mydas Komoroske et al., 2011
Ag, Sn
Tursiops truncatus Hg Pompe-Gotal et al., 2009
Stenella coeruloalba Hg Pompe-Gotal et al., 2009
Several studies across the globe show that heavy metal pollution can
accumulate in different marine and freshwater organisms (Table 1) as a result of
bioaccumulation and can be toxic to organisms at higher trophic levels. Although
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bioaccumulation of metals are said to be species specific, at least in fish species

(Kumar & Achyuthan, 2007), this accumulation of heavy metals may have an
influence on the physiological processes of marine organisms while some even
experience morphological alterations. According to Zou et al. (2014), it was
observed that acute copper exposure (47M in 24 hours) of Sargassum fusiformes
may inhibit its photosynthetic capacity thereby reducing its carbohydrate
production. In the same study, ascorbate underwent a 90% decrease in the
S. fusiformes subjected to acute copper exposure and could have an effect on
the antioxidant system of the said organism. In diatoms, exposure to heavy
metals led to the reduction of carbohydrates and proteins, and morphological
alterations were also observed (Anantharaj, Govindasamy, Natanamurugaraj, &
Jeyachandran, 2011). In addition, fishes exposed to combinations of different
heavy metals, mercuric chloride and lead acetate showed severe pathological
changes in the gills and liver that was detrimental to the organism (Vinodhini &
Narayanan, 2009; Chavan & Muley, 2014). Heavy metal exposure of sea urchins
has also resulted to malformations in their embryo and larval form (Soualili,
Dubois, Gosselin, Pernet, & Guillou, 2008; Dermeche, Chahrour, & Boutiba,
2012). Although in other organisms, heavy metal contamination was observed
to be non-lethal (e.g. Chelonia mydas) (Komoroske et al., 2011) or cannot be
implicated as the sole reason for physiological changes in marine organisms, the
effects of heavy metals on mortality of marine organisms cannot be ruled out
(Das et al., 2003). One effect of heavy metals is its effect on the immune system
of marine mammals. Immunosupression and autoimmume diseases, for example,
could result in marine mammals exposed to metal pollution (Kakuschke &
Prange, 2007).
Heavy metals and marine biodiversity

Several studies reviewed showed that heavy metals are negatively correlated
to marine biodiversity. A study conducted by Takarina and Adiwibowo (2011)
showed that the higher the concentration of heavy metals, the lower the diversity
of polychaete and mollusc observed. In addition, species richness of fouling
organisms, both native and non-native species, were found to have decreased
as the level of copper contamination increased, both in tropical and temperate
sites (Canning-Clode et al., 2011). The result of these studies corroborates the
findings of Lacuna et al., (2013) in their study on foraminiferal assemblage.
The study showed lower foraminiferal biodiversity on sites that were exposed to
effluents from a ferro-nickel smelting plant. The said study site were dominated
by a pollution-tolerant species and the authors stated that the low diversity could
123
have been caused by the effluent that was coming from the metal smelting plant.
Figure 1. Marine debris accumulation sites in the worlds

oceans showing the 6th Possible garbage patch in Barents Sea
(van Sebille, England, & Froyland 2012)
Plastic pollution
Marine debris is a global problem that can affect marine organisms, ecological
processes, aesthetics and economies (Smith & Markic, 2013). It is recognised
globally as a key threatening process to marine life (Smith & Edgar, 2014).
As defined by Secretariat of the Convention on Biological Diversity and the
Scientific and Technical Advisory PanelGEF (2012) Marine debris is any
persistent, manufactured or processed solid material discarded, disposed of, or
abandoned in marine and coastal environment. This definition encompasses a
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myriad of products that can be classified under four main types of materials such
as glass, metal, paper and plastic. Other definition of marine debris also includes
organic materials, which were the dominant marine debris before the production
of plastics and other synthetic materials (Shealvy, 2005).
Of all marine debris, plastics represent the vast majority of man-made
debris in marine environment (Allsopp, Walters, Santillo, & Johnston, 2006;
Barnes, Galgani, Thompson, & Barlaz, 2009; Reisser et al., 2013; Czar et al.,
2014). Plastic can be a range of different types of hydrocarbon polymers, with
polyethylene as the most commonly used plastic (Andersson, 2014). Other
plastic includes polystyrene, nylon and polyvinyl chloride (Andrady, 2003). Ryan
(2013) observed man-made marine debris were roughly two orders of magnitude
more abundant than natural debris such as coconuts and cuttlefish shells. Due
to its durability and slow degradation, plastics have higher residence time in
the marine environment thereby causing the accumulation of these materials in
different oceans in the world (Figure 1) (Law et al., 2010; van Sebille et al., 2012;
Eriksen et al., 2013; Reisser et al., 2013; Czar et al., 2014) and replacing organic
materials as the most common marine debris (Shealvy, 2005). In the Straits of
Malacca and Bay of Bengal, plastic debris was found to compose 98% of the
more than 18,000 debris materials collected in both areas (Ryan, 2013). A study
conducted by Czar et al. (2014) found that plastic had 88% occurrence in all
the samples that they collected from different parts of the world and places their
estimate on the amount of plastic debris in open-ocean surface to be at 7,000 to
35,000 tons, while an estimate from Eriksen et al. (2014) further places plastic
pollution at 268,940 tons or 5.25 trillion plastic particles. This data on plastic
debris may have been underestimated since Reisser et al. (2013) suggest that
biofouling may cause soft plastics to sink and the possibility some plastics were
not included in the collection is present. Moreover, there are also plastic debris,
such as PVC and nylon, that do not float leading to further underestimation
of plastic in the marine environment (Allsopp et al., 2006). An estimate on
the density of marine debris in deeper sea floors puts the value at 2700 pieces
per square kilometre in the ABC-islands, Dutch Caribbean alone, with plastic
making 29% of the total materials collected (Debrot, Vinke, van der Wende,
Hylkema, & Reed, 2014). A study conducted by Galgani, Souplet, and Cadiou
(1996) in the French Mediterranean Coast, has placed plastic debris to as high as
at least 90% of the total debris. Also, in Greece, plastics also make up majority
of marine debris on the sea floor, 79% and 83% of the collected debris in two
different enclosed gulfs (Stefatos, Charalampakis, Papatheodorou, & Ferentinos,
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1999). In association with these in Argentina, a survey that was conducted in river
and estuary bottoms have yielded plastics as the most important anthropogenic
debris amounting to 77% of the total number of debris, constituting to 74% of
the total weight of debris (Acha et al., 2003). These studies corroborate that in
different parts of the globe, plastics comprise a large percentage of marine debris
found in seafloors.
Plastics also undergo UV degradation, biodegradation, ingestion by marine
animals and fragmentation to smaller microplastics which puts these estimates
on the amount of plastic pollution at the conservative level (Cozar et al., 2014;
Eriksen et al., 2014). Plastics, especially microplastics, are also being incorporated
into food webs, getting passed on from lower trophic levels to higher trophic
level through ingestion. Evidence of this trophic transfer of plastic was shown
by Farrell and Nelson (2013), in which mussels (Mytilusedulis) that were fed
with microplastics were found to transfer these items to a crab (Carcinusmaenas)
that fed on the mussels. Furthermore, trophic transfer of microplastic was also
observed in planktonic food webs, where these materials were transferred from
mesozooplankton to macrozooplankton (Setl, Sopanen, Autio, Kankaanp, &
Erler, 2011). Plastic stored in biomass of marine organisms adds to the removal
of plastic from the ocean surface, leading to further underestimation.
Sources of Marine Plastic Pollution

Sources of plastic pollution are identified as either land-based or ocean-based
(Derraik, 2002; Sheavly, 2005; Gago, Lahuerta, & Antelo, 2014; Cozar et al.,
2014). For the purpose of this review, only the land-based sources of marine
plastic pollution will be discussed.
Plastic pollution enters the ocean mainly from land-based sources. Around
80% of plastic pollution in marine environment was estimated by Faris and Hart
(1994) to have been coming from terrestrial sources and the remaining 20%
were assumed to be coming from maritime activities (Lebreton et al., 2012).
Plastic pollution is observed to be higher in densely populated areas where there
are higher anthropogenic activities. The estimate of Faris and Hart (1994) is
corroborated by the study of Ryan (2013) that suggested that the concentration
of marine litter found in the Straits of Malacca peaks at areas just off urban
centers, such as Kuala Lumpur in Malaysia, and Lhokseumawe and Banda Aceh
in Indonesia. Furthermore, in Australia, it was observed that there was higher
number of plastic materials in marine areas near cities (Reisser et al., 2013) and
in New Zealand, the area that had the greatest concentration of plastic pollutants
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are near industrial centers (Gregory, 1978). A study conducted Nova Scotias
Halifax Harbour (Walker, Grant, & Archambault, 2006) have shown that the
majority of marine debris found in its intertidal beach were waste generated from
recreational activities. Moreover, the high presence of packaging materials and
plastic bags as marine debris further supports the idea that land-based sources
are primarily the source of plastic in the marine environment (Derraik, 2002;
Ryan, 2013).
Plastic is transferred from terrestrial to marine environments through several
ways. Shealvy (2005) has identified three pathways, namely, sewer overflows
and sewage treatment plants, shore-based solid waste management and through
littering.
According to UNEP (1999), shore-based solid waste management, such
as landfills or open waste dumps, contributes plastic in marine environments.
Poorly managed or illegal landfills contribute to plastic waste either by plastics
getting blown by the wind or when the landfills get flooded and, therefore, carry
plastic debris to rivers and inland bodies of water (Hoellein, Rojas, Pink, Gasior,
& Kelly, 2014). This will in turn, bring the plastic materials to sea. Plastic can be
directly transferred to the sea from landfills that have close proximity to the sea.
Moreover, sewage treatment plants and sewerage facilities is also considered to be
a contributor to marine plastic pollution, as mentioned by Shealvy (2005), the
overflow of these sewage treatment facilities moves debris towards the sea during
flooding. Littering on the streets, gutters, sidewalk, in coastlines and beaches by
people contributes to marine debris (Walker et al., 2006; Bergmann & Klages,
2012; Gago et al., 2014). According to OSPAR Commission (2009), marine
litter in coastlines in the OSPAR region is 542 items per 100m. These materials
are carried by the wind or water flow and will eventually become marine debris (
Sesini, 2011; OSPAR Commission, 2007).
Effects of plastics on marine ecosystems

Plastic debris causes detrimental effects to different marine ecosystems and
damage habitats. One is by causing physical damage to the marine habitat due
to the movement of marine plastic debris by wave action and tides (Shealvy,
2005). Marine debris can cause a smothering effect on marine organisms, such
as seagrasses and corals, impeding gas exchange or by blocking sunlight (Baulch
& Perry, 2012). These can cause the decline in the abundance and diversity
of seagrass and corals that are known to provide habitats for different marine
organisms. The effect of plastic debris on these key species will possibly cause a
decrease on the stability of ecosystems since key species create stable conditions
127
for other organisms in a community (Falkenberg, Russell, & Connell, 2012).

Another reason is that these materials can be the means of transport for non-
native and potentially, invasive organisms.
Evidence of long distance transport of marine debris was suggested by Gregory
(2009) increasing potential transport of alien species. In the study of Reisser
et al. (2014) showed that plastic pollutants collected came from domestic and
international inputs. Presence of increasing plastic debris in areas with less or no
human activity is an evidence that this material can be transported across oceans
(Bergmann & Klages, 2012) and with evidence of biofouling for plastic materials
that have been in the oceans for long periods of time (Gregory, 2009; Zettler
et al., 2013), movement of possible invaders is inevitable. Invasive alien species
are organisms introduced to an area outside their normal distribution where it
will proliferate due to a host of different factors ( Chenje & Mohamed-Katerere,
2006; Cebrian & Rodrguez-Prieto, 2012; Galiana et al., 2014). Information
compiled by Molnar et al., (2008) have placed marine invasive species at 329
organisms, but these invasive species did not include organisms that can be
transported by plastic debris, therefore, an increase from this estimate is possible
as plastic debris is increasing (Sigler, 2014).
A study by Capps and Flecker (2013) found that the presence of non-native
species caused an increase in biogeochemical activity that potentially alters the
nutrient dynamics of the colonized environment. An example of alteration
of nutrient dynamics is the high faecal deposition of non-native species in
colonized environment, due to very high number of individuals, could lead to
eutrophication (Rehfisch et al., 2010).
Carson et al. (2013) have studied the plastics in the North Pacific Gyre
and found that plastic debris host a variety of microorganisms such as bacteria,
diatoms and dinoflagellates. The result of the study was corroborated by Reisser
et al. (2014) in which they showed that plastic debris provides a pelagic habitat
for smaller marine organisms that can aid in the dispersal of these organisms to
other ecosystems and could potentially become an invasive alien species that will
have a negative effect on native species, biodiversity, and ecosystem functioning
(Gregory, 2009; Katsanevakis et al., 2014).
In addition, invasive species have the capability to alter habitat and community
structure that may lead to overall biodiversity loss (Rehfisch et al., 2010). Decline
in species richness due to loss of habitat structure can result in invasion of other
species that may amplify the effects of habitat loss (Airoldi et al., 2008) or lead to
simplification of food webs thus promoting more species loss which could lead
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to more invasions (Galiana et al., 2013). Biodiversity loss leads to an exponential

decrease of ecosystem services and can impair the capacity of oceans to provide
food, maintain water quality and resiliency (Worm et al., 2006).
On the other hand, plastics increases habitat heterogeneity (Bergmann &
Klages, 2012) in the different marine ecosystems that can provide habitat for
different species. In this case, plastic could promote an increase in biodiversity
(Secretariat of the Convention on Biological Diversity and the Scientific and
Technical Advisory PanelGEF 2012). But the increase in habitat heterogeneity
can promote the existence of non-native species (Chenje & Mohamed-katerere,
2006) with negative effects already stated.
Effects of plastics on marine organisms

Plastic debris pose a threat to the survival of marine organisms either through
ingestion, entanglement, or by bringing potential invasive species, among others (
Moore et al., 2010; Schuyler et al., 2012; Reisser et al., 2013 ). There is a 40% rise
in the number of species reported to be affected by marine debris, from 247 species
in 1997 to 663 species (Secretariat of the Convention on Biological Diversity
and the Scientific and Technical Advisory PanelGEF 2012). Plastics can have
sub-lethal to lethal effects on marine organisms (Table 2). The increase in the
abundance of plastic in the marine environment has increased its bioavailability
(Williams, Ashe, & OHara, 2011; Wright, Thompson, & Galloway, 2013).
Marine debris are known to accumulate in distinct regions around the globe
following the oceanic currents (Figure 1). The ingestion of marine debris such
as plastics have been proven to be fatal to most of marine organisms such as
marine turtles, cetaceans and seabirds ( Provencher et al., 2010; Lazar & Graan,
2011; Schuyler et al., 2012). These organisms may mistakenly take plastics as
their prey item (Schuyler et al., 2012; Lavers et al., 2014) or accidentally ingest
plastic together with their prey (Choy & Drazen, 2013; De Stephanis et al.,
2013). Effects of plastic ingestion include lacerations to the internal organs and
blockage of the digestive tract, for example, can cause mortality (De Stephanis
et al., 2013). In addition, these debris may disrupt physiological functions in
organisms due to chemicals sorbed into it (Hirai et al., 2011; Teuten et al., 2009).
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Table 2. Plastic ingestion of organisms and its effects.(EN = Endangered; CE

= Critically Endangered; VU=Vulnerable; LC = Least Concern; DD = Data
Deficient)
Effects of Plastic IUCN Status and
Species References
Debris Ingestion Population Trend
Marine turtles
Eretmochelys imbricata
Not determined CE (decreasing) Schuyler et al., 2012
(Hawksbill turtle)
Schuyler et al., 2012;
Chelonia mydas (Green
Not determined EN (decreasing) Mascarenhas et al.,
turtle)
2004
Lepidochelys olivacea (Olive Mascarenhas et al.,
Not determined VU (decreasing)
Ridley turtle) 2004
Carretta carretta
Mortality EN (unknown) Lazar and Gracan 2011
(Loggerhead turtle)
Marine Mammals
Di Beneditto and
Pontoporia blainvillei
Non-lethal VU (decreasing) Ramos 2014; Denuncio
(Franciscana dolphin)
et al., 2011
Sotalia guianensis (Guiana Di Beneditto and
Non-lethal DD (unknown)
dolphin ) Ramos 2014
Gastric rupture
Physeter macrocephalus Jacobsen et al., 2010; de
following impaction VU (unknown)
(Sperm whale) Stephanis et al., 2013
with debris; lethal
Kogia breviceps (pygmy Stomach occlusion Tarpley and Marwitz
DD (unknown)
sperm whale) ; lethal 1993
Balaenoptera acutorostrata Tarpley and Marwitz
Not determined LC (stable)
(Minke whale) 1993
Phocoena phocoena (Harbour Blockage of the
LC (unknown) Baird & Hooker, 2000
porpoise) esophagus
Indopacetus pacificus Blockage of the
DD (unknown) Kaladharan et al., 2014
(Longmans beaked whale) digestive tract
Creates a false
Mesoplodon densirostris
sensation of fullness DD (unknown) Secchi and Zarzur 1999
(Blainvilles beaked whale)
leading to emaciation
Obstruction of
Ziphius cavirostris (Cuviers
digestive tract leading LC (unknown) Gomercic et al., 2006
beaked whale)
to starvation
Obstruction of
Tursiops truncatus
digestive tract leading LC (unknown) Levy et al., 2009
(Bottlenose dolphin)
to starvation
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Marine Birds
Pachyptila desolata
Non-lethal LC (decreasing) Auman et al., 2004
(Antarctic Prion)
Reduction of
Puffinus carneipes (Flesh-
stomach capacity; LC (stable) Lavers et al., 2014
footed Shearwater)
non-lethal
Uria lomvia (Thick-billed
Not determined LC (increasing) Provencher et al., 2010
Murre)
Non-lethal; plastic-
Puffinus tenuirostris (Short-
based chemicals LC (decreasing) Tanaka et al., 2013
tailed Shearwater)
transferred to tissues
Calonectris diomedea (Corys
Non-lethal LC (decreasing) Rodriguez et al., 2011
shearwater)
Marine Fishes
Lampris sp. (big-eye Anela Choy & Drazen,
Not determined Not known
moonfish) 2013
Lampris sp. (small-eye Anela Choy & Drazen,
moonfish) 2013
Alepisaurus ferox (longnosed Anela Choy & Drazen,
Not determined LC (Unknown)
lancetfish) 2013
Coryphaena hippurus Anela Choy & Drazen,
Not determined LC (Stable)
(Common dolphinfish) 2013
Gempylus serpens (snake Anela Choy & Drazen,
mackerel) 2013
Thunnus obesus (big-eye Anela Choy & Drazen,
Not determined VU (decreasing)
tuna) 2013
Xiphias gladius (broadbill Anela Choy & Drazen,
Not determined LC (decreasing)
swordfish) 2013
Symbolophorus californiensis Not determined Not known Boerger et al., 2010
Myctophu maurolanternatum Not determined Not known Boerger et al., 2010
Loweina interrupta Not determined Not known Boerger et al., 2010
Hygophum reinhardtii Not determined Not known Boerger et al., 2010
Astronesthes indopacifica Not determined LC (unknown) Boerger et al., 2010
Cololabis saira Not determined Not known Boerger et al., 2010
Marine Invertebrates
Lepas sp. (Gooseneck
Not determined Not known Goldstein et al., 2013
barnacles)
Arenicola marina
Not determined Not known Teuten et al., 2007
(Lugworm)
The IUCN Red List of Threatened Species. Version 2014.3. <www.iucnredlist.org>.
Downloaded on23 March 2015
131
Effects of plastics on marine birds

Mortality of vertebrates has been reported to have occurred due to ingestion
of plastic litter. Although it is difficult to prove that the ingestion of plastic was
the cause of death (STAP, 2011), circumstantial evidences point to plastic as
the reason for their demise. Adult marine birds ingest plastic floating in marine
environment mistaking these materials as their prey (Lavers, 2014) while
juveniles and fledglings ingest food through parental transfer (Rodrguez et
al., 2011). In a review conducted by Azzarello and Van Vleet, (1987), plastic
ingestion by marine birds have been observed in several species and one species,
Diomedea immutabilis (Laysan albatross), more than 90% of carcasses contained
anthropogenic debris with plastics comprising approximately 30% (Kenyon
& Kridler, 1969). Moreover, Provencher et al., (2010) have also recorded that
approximately 11% of the specimen of Thick-billed Murre (Uria lomvia) that
were collected in the Canadian Arctic had plastic in their digestive system.
Ingestion of plastic can result to obstruction in the intestines and ulcerations in
the mucosa of the proventriculus (Pettit et al., 1981).
Moreover, plastic in the stomachs of these birds may affect the feeding habit
and activity by suppressing hunger stimulants, such as stomach contractions
(Azzarello & Van Vleet, 1987). To simulate the effect of plastic on the feeding
behaviour of sea birds, an experiment by Ryan (1988) on Gallus domesticus has
showed a decrease in meal size after the chicken were fed plastic pellets due to
the reduction of stomach capacity. In fact, flesh-footed shearwater fledglings
were observed to have significant body mass reduction and wing chord and head
bill length as the plastic loads increased. The plastic possibly contributed to low
nutrient uptake due to the decrease in stomach capacity resulting to negative
effects on survival of juvenile birds and ultimately, the population viability of
flesh-footed shearwaters (Lavers 2014). Aside from these, plastic in the stomachs
of marine birds can also have a physiological effect on the secretion of digestive
enzymes, and reproduction due to the presence of chemicals that may delay
ovulation (Peakall, 1970; Day, 1980).
Effects of plastics on marine turtles

The incidence of ingestion of plastic by marine turtles is due to the organisms
mistakenly taking plastics as their prey item (Sigler, 2014). In a study conducted
by Schuyler et al., (2012), turtles seems to be favouring the ingestion of plastic
that is either white or transparent, which is thought to resemble its preferred prey
(e.g. jellyfish), although some species are known to feed indiscriminately due to
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its generalists feeding behaviour which results to ingestion of different plastics

(Tomas et al., 2002) which raises concern on the increasing availability of plastics
to these marine organisms. Stomachs of Caretta caretta (loggerhead turtles) in
the Adriatic Sea contained different types of plastic materials with plastic bags
and wrapping foils having the highest percentage at 68.4% (Lazar & Grocan,
2011). In another study 33.9% of turtle specimen, both Chelonia mydas (Green
turtle) and Eretmochelys imbricate (Hawksbill turtle), were found to have ingested
marine debris, with plastic having the greatest percentage (Schuyler et al., 2012).
Moreover, in a study conducted on Dermochelys coriacea (Leatherback turtle),
plastics were observed to be present in the gastrointestinal tract in 33.8% of
all the specimen (Mrosovsky, Ryan, & James, 2009). Although deaths of these
turtles are not known to have been caused by the ingestion of plastics, these
materials were found to be causing blockage of the gastrointestinal tracts (Sigler,
2014), and blockage of the gut due to plastic to an extent can be considered
lethal to these turtles (Mrosovsky , Ryan, & James, 2009). This lethal effect of
plastic ingestion is corroborated by the study of Lazar and Gracan (2011) in
which turtle carcass did not show any signs of any external stresses and implicated
that the mortality was caused by the presence of plastic in the gastrointestinal
tract. Ingestion of plastic and accumulation thereof, also have sub-lethal effects
to these marine organisms, which includes lesser food intake which results to
lower energy leading to decreased growth rate, longer developmental periods,
reduced reproductive output and increases vulnerability to predation (McCauley
& Bjorndal, 1999; Mrosovsky et al., 2009; Plot & Georges, 2010).
Effects of plastics on marine mammals

Although ingestion of small plastics in small amounts in some marine
mammals showed no deleterious effect (Di Beneditto & Ramos, 2014) reports
on the incidence and effects of plastic ingestion are numerous. Moreover, plastic
are also reported to have caused mortality on marine mammals. There are at
least 26 species of cetaceans documented to have ingested marine plastic litter
(Baird &Hooker, 2000; Bearzi et al., 2011; Denuncio et al., 2011). The threat
of plastic to marine mammals could be attributed to the increase encounter of
these mammals with these pollutants (Williams et al., 2011). Marine mammals
does not select plastics as their prey item (Secchi & Zarzur, 1999) unlike other
marine vertebrates that easily mistaken plastics as their prey (e.g. turtles and
birds), instead, plastics may be ingested together with their prey (Sigler, 2014),
so an overlap in their distribution and the distribution of plastics as shown by
133
Williams et al., (2011), could elevate the chances of these accidental ingestions.
As mentioned by Beneditto and Ramos (2014), there was more marine debris
in the stomach of coastal dolphin Pontoporia blainvillei since its feeding area
is littered with plastic compared to another species of coastal dolphin, Sotalia
guianensis, which had different feeding habit.
In India, Indopacetus pacificus (Longmans beaked whale) was found to
have ingested plastic bags. The whale did not exhibit any external damages or
lesions, which places the ingestion of plastic as the main cause of its mortality
(Kaladharan et al., 2014). A similar case was observed by (Tarpley & Marwitz,
1993) in two different species of cetaceans. Two Pygmy sperm whale and a Minke
whale possibly succumbed to the lethal effects of plastic ingestion. Result of the
necropsy of the three whales showed that one of the Pygmy sperm whale died
of multiple active ulcerations throughout its stomach, while the other Pygmy
sperm whale and the Minke whale was shown to have ingested plastic bags that
have caused blockage in its digestive tract. Blockage in digestive tracts of different
cetaceans were observed by Gomeri et al. (2006), Jacobsen, Massey, and
Gulland (2010) and Baird and Hooker (2000). The authors hypothesized that
the presence of plastic bags in cetacean stomachs resulted to starvation. Ingested
plastic may also cause false sensation of fullness, that may lead to smaller meal
size, causing the whale not to meet its energy requirement and eventually lead to
its demise (Secchi & Zarzur, 1999).
Trophic transfer of the harmful effects of marine plastic debris

Microplastic is identified as one of the emerging global issues (Sutherland
et al., 2010). Microplastic is defined as pieces or fragments of plastics that has a
size less than 5 mm (STAP, 2011).One source of this marine debris is through
the mechanical breakdown of large plastics(Thompson et al., 2004). Plastics at
sea may also undergo photodegradation that results to weathering and would
cause plastic constantly exposed to sunlight to become brittle (Andrady, 1990).
Another source of microplastic is from domestic scrubbing and beauty products
such as facial cleansers that contain polyethylene microplastics or the so-called
microbeads (Fendall & Sewell, 2009). The ingestion and the transfer of these
microplastics from one trophic level to the next could cause bioaccumulation
and biomagnifications that can have deleterious implications (Farrell & Nelson,
2013).
Furthermore, plastic have sorption capacity for heavy metals (Rochman
et al., 2014) and different organic micropollutants such as polychlorinated
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biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), dichloro-diphenyl-

trichloroethane and its metabolites (DDTs), polybrominateddiphenyl ethers
(PBDEs), alkylphenols and bisphenol A (Hirai et al., 2011), and organohalogen
(Karlsson et al.,2006)that are deleterious to physiology of marine organisms. In
fact, sorption of pollutants, such as heavy metals and phenanthrene, are higher in
plastic than in natural sediments and sea water particulates (Teuten et al., 2007;
Rochman et al., 2013), leading to the idea that plastic acts as trap for pollutants
(Rios, Moore, & Jones, 2007; Andersson, 2014).
Moreover, plastic in the marine environment may also have the capability
to release these sorbed materials when moved to an area where there is less
concentration of pollutants (Teuten et al., 2007). Heavy metals that is considered
to be primary pollutants by the United States Environmental Protection Agency,
such as (Cd, Ni, Zn and Pb), were found to be present in different types of
plastic debris in marine environment. In addition, Fries and Zarfl (2012)
demonstrated that both high-density and low-density polyethylene plastics has
sorption capabilities for polycyclic aromatic hydrocarbons, making transport
possible (Teuten et al., 2007), increasing its bioavailability Plastic concentrates
toxic materials and serves as a pathway for these toxic pollutants into marine food
webs (Engler, 2012).
With all these pollutants present in plastics in the marine environment,
ingestion by marine organisms poses a great threat. These pollutants are not
irreversibly bounded to plastics, making bioaccumulation and biomagnification,
in animals that ingest these possible (Andersson 2014). Rochman et al. (2013)
have observed that fishes who were fed with tainted plastic tend to accumulate
chemicals in their body. Engler (2012) mentioned that surfactants in the guts
of deposit feeders have the capability to mobilize pollutants sorbed to plastics.
Thus, making them available for the organism. Teuten et al., (2009) observed
that pollutants, such as polychlorinated biphenyls, could transfer from plastic
towards an organism. Furthermore, benthic organisms, such as lugworms
(Arenicola marina), incorporates pollutants, such as phenanthrene, to its biomass
(Teuten et al., 2007) while mussels (Mytilus edulis) showed that translocation of
microplastic particles to its circulatory system was possible (Browne et al., 2008).
A study conducted by Tanaka et al. (2013) also showed that plastic-derived
chemicals from ingested plastic were also found in the adipose tissues the
organism and there was a higher concentration of pollutants in organisms that
ingested plastic than those that did not (Yamashita et al., 2011). Due to this,
the possibility of bioaccumulation and trophic transfer of plastic debris and its
135
toxic components is not far-fetched and there are now experimental evidence
that support the occurrence of such events. In an experiment, fishes were fed with
plastic, both contaminated and uncontaminated with organopollutants, showed
that there was higher concentration of pollutants (e.g. PAHs, PCBs & PBDEs)
in fishes that were fed plastics with organopollutants (Rochman et al., 2013).
Furthermore, it was also observed that there was an increasing trend in the
concentration of organic pollutants as the size of fishes increased. Harmelin-
Vivien et al., (2012) showed there was higher concentration of organic pollutants
for fishes that feed on larger prey than those that feed on smaller prey which
would imply that there is biomagnification of these pollutants on plastic. The
idea of prey transferring plastic and its pollutants to its predator was observed by
Takeuchi et al. (2009) in seals. Results suggest that seals do not directly ingest
plastic pollutants. However, they consume fishes that feed on plastic leading to
the increase of pollutants in Seal fat tissues. In addition, lobsters that were fed
with fishes tainted with plastic were found to accumulate the plastic materials in
their bodies up to at least 24 hours (Andersson, 2014).
Plastic and infectious diseases

Plastic can serve as a vector for diseases since potential pathogenic
microorganisms thrive in these pelagic habitats that can have detrimental effects
to organisms that consume them. Zettler, Mincer, and Amaral-Zettler (2013)
detected the dominance of Vibrio sp. in microplastic collected. The ingestion
of these plastic marine debris has the possibility of transferring these potentially
pathogenic microorganisms, especially when the organisms that ingest these
plastic materials were shown to have the capability to become reservoirs and
vectors of infectious diseases. For example, Vibrio cholerae, a human pathogen,
were detected in different fish species making them reservoirs and possible
vectors of the disease (Senderovich, Izhaki, & Halpern, 2010). Although linkages
between the transfer of pathogens from plastics towards the organism that ingest
it has not been documented, this merits further investigation.
Implications to Philippine marine biodiversity

The Philippines hosts very high diversity of marine organisms (Carpenter &
Springer, 2005). Data from Fishbase (2008) and Bureau of Fisheries and Aquatic
Resources (BFAR) and the National Fisheries Development Institute (NFRDI)
and Protected Areas and Wildlife Bureau (PAWB) (2005) stated that the country
has 468 scleractinian corals, 1755 reef-associated fishes, 648 species of molluscs,
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Volume 15 July 2015
19 species of sea grasses and 820 species of algae as cited (Philippine Biodiversity
Conservation Priority Setting, 2010). Sadly, the Philippines is also considered a
biodiversity hotspot, where there is a rapid decline in the biodiversity of the
country (Roberts et al., 2002; Naola, Alio, & Carpenter, 2010) and pollution
is going to make it decline more.
In the Philippines, 81% of provinces are coastal with a total of 832 coastal
municipalities and coastlines have a population density of 286 persons/km2
with an estimated growth of 2.3% annually (PEMSEA 2015). As of 2010,
the Philippines have a population of more than 92 million and is estimated to
reach over 120 million by the year 2025 (PSA-NSO, 2012). Urban centres in
the Philippines are also densely populated with National Capital Region (NCR)
population density at 18,642 people/km2. This increase in population is coupled
by increase in demands for food and shelter leading to coastal developments to
accommodate this need.
To address the increasing demand for food, culturing of freshwater and marine
species have been adapted. Aquaculture produced 51.7 million tonnesof aquatic
and marine organisms in 2006 (FAO, 2015). In the Philippines, Primavera (2006)
reported that there is an observed >50% decline of mangrove areas from 1951-1988
and was reported to be declining at a rate of 1,400 ha per year from 1990 to 2010
(Long et al., 2014). In addition, seagrass beds have also experienced 40 % decline
(Macusi et al., 2011). Although aquaculture is not the sole cause of these declines,
its effects are significant. In mangroves, for example, Primavera (2006) reported
that 95% of brackish water ponds from 1952-1987 are mangrove area converted
for aquaculture. Intensive fish farming is implicated in the increase of nutrient
and sedimentation in the marine environment. Sediment analysis conducted by
David et al., (2008) showed that as the volume of fish cages and aquaculture
facilities increased, there was also an increase of phosphorous load. In one of the
three sites sampled in Bolinao, Pangasinan, where fish cages for milkfish culture
are numbered to be more than 1,100 , average phosphorous loading have risen to
204.2 kg/km2/yr from a high of 75.7 kg/km2/yr observed prior to aquaculture
development. This study was corroborated by Villanueva et al. (2005; 2006)
in which data showed a very high ammonium (>7 M) and phosphate (>0.8
M) loading in sites of aquaculture. With the increasing aquaculture facilities,
Philippines will experience an increase in nutrient enrichment and sedimentation
in the marine environment. Another source of sediments with high organic matter
content and nutrients in the marine environment are rivers (Woolger, 2009;
Argente et al., 2013). In a study by Chang et al. (2009) in Manila Bay showed
137
the source of these excessive nutrients are rivers that drain in the Bay. Their data
showed that there was higher concentration of nitrates and nitrites (3.04M)
in an area of Manila Bay located at close proximity to the mouths of rivers than
areas away from rivers (0.90 M and 0.10 M). This result is in conjunction to
a study conducted by Li and Daler (2004) in East China Sea where pollutants
such as inorganic nitrogen, phosphate, oil hydrocarbons, organic matters and
heavy metals were found to be coming from the Yangtze River. These studies
support the fact that nutrient enrichment and sediment deposition to marine
environment is also influenced by anthropogenic activities on land (e.g. land
clearing for agriculture, mining, urbanization) (Bartley, 2014). Studies on the
effects of sedimentation and nutrient enrichment in the Philippines have shown
negative impacts to corals, seagrasses and other marine organisms. Escobar et al.,
(2013) showed that the June 2010 fish kills in Bolinao and Anda, Pangasinan
coincided with high total inorganic nitrogen (TIN). During the fish kills, TIN
was recorded at 12.2 M, which is almost 3-folds to the ASEAN water quality
criterion of 4.40 M. Furthermore, phosphate concentration (2.37 M) during
the fish kill was also observed to be higher than the ASEAN criterion (1.45 M).
Fish kills are often a result of very low dissolved oxygen levels and is connected
with high nutrient levels. Moreover, a study conducted by Sotto et al. (2014) in
Manila Bay, have found that areas with higher nutrient concentration have lower
near-bottom dissolved oxygen level. They have recorded a dissolved oxygen (DO)
level of 0.028 mg/L during the time which total inorganic nutrients have reached
27.8 M, the highest during the sampling. This result is way below the DO level
of hypoxic waters which is at 2 mg/L (Levin et al., 2009).
Meanwhile, the effects of nutrient enrichment and sedimentation on habitat-
forming species such as seagrasses and corals are of greater concern. These
ecosystem engineers play a significant role in marine biodiversity. Vermeij et al.
(2008) showed that 98% of Ocyurus chrysurus reef population utilized seagrass
nurseries during its juvenile stage. In a study conducted by Honda et al. (2013)
in the Philippines, 29 fish species were found to utilize multiple habitats with 11
species reported to have been found utilizing seagrass beds and 15 species utilizing
corals. Habitat heterogeneity, created by ecosystem engineers (i.e. seagrass and
corals) is found to positively affect biodiversity (Cardoso et al., 2004; Hosack et
al., 2006). Nutrient enrichment and sedimentation is shown to reduce habitat
heterogeneity by either promoting dominance of a single species or by total
eradication of these habitat-forming species (Villanueva, 2005; 2006; Powell et
al., 2014). In a review conducted by Cabaco et al. (2008), seagrass are negatively
138
Volume 15 July 2015
affected by sedimentation through burial. Seagrass species like Zostera marina

were very susceptible even at low levels of burial (2-4 cm), experiencing 70-90%
mortality while Enhalus acoroides are more resistant to burial, experiencing only
40% mortality when exposed to 16cm of sediments. The review by Cabaco et al.
(2008) showed that seagrass response to burial is species specific, nonetheless, there
is an expected change in seagrass composition since species that are more resistant
to sediment burial will dominate seagrass landscape as the sedimentation in the
marine environment increases. In Bolinao, Pangasinan, the Philippines, Fortes et
al. (2012) have observed that there was a decline in seagrass species in study sites
closer to aquaculture structures. The study site closest to aquaculture sites only
had two species compared to seven seagrass species found in sites farthest from
aquaculture structures. This decrease in species richness shows domination of
two seagrass species in areas where eutrophication and sedimentation was highest.
Although the study by Fortes et al. (2012) failed to quantify the sedimentation
rates or difference in nutrient concentrations in the different study sites. In a
separate study conducted by Villanueva et al. (2005) in Bolinao, Pangasinan,
sites near aquaculture facilities experienced ten-fold increase in sedimentation
rates (20gm-2d-1 in sites farthest from aquaculture facilities to 200 gm-2d-1 in
sites near aquaculture facilities) that would support the fact that there is high
sedimentation rate in areas near aquaculture sites and seagrasses experience burial
more in areas near aquaculture sites. Burial by sediments is also a major problem
for corals. As demonstrated by Villanueva (2005; 2006), corals showed very low
survivorship in sites where sedimentation and nutrient enrichment was high.
Further, Villanueva et al. (2005) showed that aquaculture reduced water
transparency from 80% (in sites farthest from aquaculture sites) to six percent.
This reduction of transparency entails a decrease in light penetration, endangering
seagrass and coral populations. As mentioned above, these organisms have very
high light requirements for survival and increase in turbidity has been found to
have negative impacts (Fabricius, 2005; Orth et al., 2006).
Another problem that the Philippines is facing is the increasing heavy metal
pollution in the marine environment. There is very little information on the
levels and distribution of these heavy metals in the country (Velasquez et al.,
2002). A study in Manila Bay showed that land-based marine pollution has led
to an increase in heavy metal concentrations. Results showed that total cadmium
concentration was highest at a mean of 56.924 mg L-1 , followed by lead (0.743
mg L-1) and chromium (0.368 mg L-1) (Su et al., 2009). In a separate study
conducted by Velasquez et al., (2002), higher concentrations of heavy metals
139
were observed in near shore sites and sites that were facing Pampanga river.
Heavy metals were also detected in the water column near a jetty port and several
beach resorts in Iloilo, Philippines (Sarinas et al., 2013; Sarinas & Alfonsa,
2014). Both these studies registered a high concentration of heavy metals that
exceeded the allowable value by Philippine Government. The result of the study
showed that sea water near a jetty port had average cadmium concentration was
0.69 mg/L, average chromium concentration was 0.81 mg/L and average lead
concentration was 0.34 mg/L. In a different site in Iloilo, Philippines, average
chromium, lead and cadmium concentrations in sea water was 0.55 mg/L, 0.77
mg/L and 0.02 mg/L, respectively. Moreover, heavy metal contamination was
present in marine sediments in Marinduque, Philippines from a mine tailings
spill incident that occurred in 1996 (David, 2002). Although several studies
have discussed presence of heavy metals in marine environments and organisms
in the Philippines (e.g. Su et al., 2009; Solidum et al. 2013), its effects on marine
biodiversity is not placed into consideration. Heavy metals also cause biodiversity
decline due to its toxicity that cause mortality to organisms (Factor & de Chavez,
2012).
Another threat to Philippine marine biodiversity is plastic pollution. Globally,
there has been an increasing trend both in the amount of plastic debris and
number of marine organisms affected by it. In the Philippines, this increase in
plastic pollution is also evident. The amount of garbage collected from Philippine
seas has been doubling every year since 2010 and in Manila Bay alone, more
than 750 liters of marine debris are plastic with 23.2% of this being plastic bags
(Ranada, 2014). No data or records of the amount of marine plastic debris were
found for a comprehensive review in other parts of the Philippines. Further, no
reports on plastic ingestion or entanglement by marine organisms has been found
in the Philippines. This explains the inadequacy or lack of knowledge on the
extent of this problem in the country although the majority of its population is
residing on or near coastlines. Although many data were not included for lack of
them such as on amount of heavy metals and their different levels of toxicity in
the marine environment or examples of plastic ingestions of turtles and mammals
specifically in the Philippines, our study can be useful reference for exploring
those topics. Further, this review highlights the need for relevant investigations
that need to be done with regard to effect of eutrophication, heavy metals and
plastic pollution in the Philippine marine environment.
140
Volume 15 July 2015
CONCLUSIONS
Nutrient enrichment, heavy metals and plastic pollution has been found
to negatively affect marine biodiversity globally. These stressors have lethal and
sub-lethal effects on marine organisms, affecting marine biodiversity directly
or indirectly. Direct effect includes removal of individuals due to mortality
while indirect effects include habitat degradation and alteration, food web
simplification, increase alien species invasion and reduction of individual
fitness. In the Philippines, there have been few studies on effects of nutrient
enrichment, sedimentation and heavy metals on different marine species but
fewer investigations were found in relation to its effects on marine biodiversity. In
the case of plastic pollution, no studies were found to have been conducted in the
Philippines that shows the effect of this stressor to marine organisms or to marine
biodiversity as a whole even though plastic pollution pose a valid threat to marine
organisms. In general, this review may become the basis for further studies on
effects of marine pollution (nutrient enrichment, sediments, heavy metals and
plastic) on marine trophic interactions especially in the Philippine setting.
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Vol.

15 July 2015 Volume 15 July 2015

Nutrient Enrichment, Sedimentation,

CYRIL TOM B. RANARA

GLIO FLORGILEY P. ARABEJO

Gunning Fog Index: 10.15 Originality: 100% Grammar Check: 90%

Marine biodiversity plays a vital role in ecosystem resilience and stability

mortality of organisms while indirect effects include habitat degradation or

Ecology, nutrient enrichment, sedimentation, plastic, biodiversity, literature

Biodiversity promotes community stability and productivity of an ecosystem

effects of different pollutants to marine organisms and the marine environment.

OBJECTIVES OF THE STUDY

This review discussed the implications of sedimentation, nutrient enrichment,

RESULTS AND DISCUSSION

Sedimentation and nutrient enrichment

Effects of sedimentation and nutrient enrichment on corals

Effects of sedimentation and nutrient enrichment on seagrass

recruitment as new seagrasses shoots were also found to be susceptible to limited

Effects of habitat loss or alteration on marine biodiversity

Table 1. Presence of heavy metals in different marine and freshwater organisms.

bioaccumulation of metals are said to be species specific, at least in fish species

Heavy metals and marine biodiversity

Figure 1. Marine debris accumulation sites in the worlds

Sources of Marine Plastic Pollution

Effects of plastics on marine ecosystems

for other organisms in a community (Falkenberg, Russell, & Connell, 2012).

to more invasions (Galiana et al., 2013). Biodiversity loss leads to an exponential

Effects of plastics on marine organisms

Table 2. Plastic ingestion of organisms and its effects.(EN = Endangered; CE

Effects of plastics on marine birds

Effects of plastics on marine turtles

its generalists feeding behaviour which results to ingestion of different plastics

Effects of plastics on marine mammals

Trophic transfer of the harmful effects of marine plastic debris

biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), dichloro-diphenyl-

Plastic and infectious diseases

Implications to Philippine marine biodiversity

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