Ocean and Coastal Management 225 (2022) 106223

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Ocean and Coastal Management

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

Problems in paradise: Mangrove bird communities impacted by litter in

Jakarta Bay, Indonesia
Nurul L. Winarni a, b, *, Dimas H. Pradana a, Selsa A. Ayujawi a, Naila Zackeisha b,
Bhisma G. Anugra a, b, Yulia Wulandari b, Dalily Syachrudin b
a
Department of Biology, Faculty of Mathematics and Natural Sciences Universitas Indonesia, Kampus UI Depok, Depok, 16424, Indonesia
b
Research Center for Climate Change-Universitas Indonesia, Gd. Multidisiplin FMIPA-UI Lt. 7, Kampus UI Depok, Depok, 16424, Indonesia

A R T I C L E I N F O A B S T R A C T

Keywords: Human activities in Jakarta City, Indonesia, produce huge quantities of litter, much of which is dumped in
Index of waterbird community integrity mangrove habitats along the coast of Jakarta Bay. We identified three mangrove sites that contained no litter to
Jakarta Bay varying amounts of litter and assessed its effect on the bird communities that are associate with those mangroves.
Mangroves
We conducted this survey to determine how many birds are living with litter, and what sort of litter it is, and its
Litter
impact on bird species during October–November 2020. The study sites were Arboretum Muara Angke (AMA),
Waterbirds
Management Angke-Kapuk Protection Forest, (Hutan Lindung Angke-Kapuk, HLAK), and Angke-Kapuk Nature Recreation Park
Policy (Taman Wisata Alam Angke-Kapuk, TWAAK). We also calculated the Index of Waterbird Community Integrity
(IWCI) at each site and determined its relationship to litter. This index has been used previously to study the
impact of anthropogenic disturbances. Litter identified in the study areas mostly consisted of plastic, followed by
processed wood and rubber. Most of the litter was stranded suggesting that the mangrove roots retain litter. Of
the 28 species co-occurring with litter, 10 were waterbirds. Only two species, Oriental darter (A. melanogaster)
and Milky stork (M. cinerea), were never present where there was litter, showing a significant negative corre­
lation with litter. The IWCI was highest in AMA, followed by TWAAK and HLAK. Litter also has no correlation
with the IWCI, but the IWCI tended to be lower wherever litter was found in higher quantities. When monitor
regularly, the decreasing values of IWCI would be useful as an alarm for an improvement in the litter man­
agement by considering the different types of mangroves based on hydrological conditions. At the end, the
management activities of mangrove as part of Ramsar and litter management should be integrated.

1. Introduction
Just like humans, litter is almost everywhere in the world on land
and in the oceans. Litter is anthropogenically produced materials in the
form of debris and rubbish, which has been improperly discarded. Litter
ranges from plastic bottles, bottle caps, cigarette butts, all the way to
abandoned furniture and processed wood (Ong and Sovacool, 2012).
More than 150 countries generated 275 million metric tons (MMT) of
plastic litter in 2010. Plastic is persistent, taking a long time to break
down into small particles called microplastics. This has a severe impact
on the environment and wildlife (Özdilek et al., 2006). When entering
the ocean, plastic debris can be mistakenly ingested by marine organ­
isms and can damage marine ecosystems (Jambeck et al., 2015). As
much as 4.8 to 12.7 MMT of plastic litter flows into the ocean (Jambeck
et al., 2015). As the disposal or removal of litter such as plastic, glass,
aluminium and other metals is difficult, waste management has become
a severe problem for many countries, especially developing countries
such as Indonesia (Thompson et al., 2009; Worm et al., 2017). Indonesia
is ranked second after China in mismanaged plastic litter with 3.22
MMT/year and dumping plastic litter as marine debris with 0.48–1.29
MMT/year (Jambeck et al., 2015). Jakarta City, with a population of
10.56 million (BPS, 2021) in the metropolitan area, dumps large
quantities of household rubbish, electrical waste, and construction and
demolition debris into adjacent natural habitats associated with rivers
and the ocean.
Human disturbances in coastal areas have increased greatly due to
the increasing human population, with more than 30% of the world’s
people living along the coastline within 0–100 m above sea level (Cohen
and Small, 1998). This is exactly the situation in Jakarta, the capital of
Indonesia. It is a coastal city on Java Island, the 13th largest island in the

* Corresponding author. Department of Biology, Faculty of Mathematics and Natural Sciences Universitas Indonesia, Kampus UI Depok, Depok, 16424, Indonesia.
E-mail address: nwinarni@gmail.com (N.L. Winarni).

https://doi.org/10.1016/j.ocecoaman.2022.106223
Received 1 October 2021; Received in revised form 10 May 2022; Accepted 10 May 2022
Available online 25 May 2022
0964-5691/© 2022 Elsevier Ltd. All rights reserved.
N.L. Winarni et al.
world, which has a population of over 152 million, representing more
than half of the whole Indonesian population making it the most densely
populated island in Indonesia (BPS, 2021). The coastal parts of Jakarta
Bay, on the northern side of the metropolitan area adjacent to the
harbour, are densely packed with human settlements, hotels and some of
the major recreation facilities within Jakarta. Jakarta Bay is an estuary
at the mouth of three main rivers, Cisadane, Angke, and Citarum. All the
litter from the river catchments, including household rubbish as well as
agricultural and commercial litter is brought daily to the coast, and
ocean, even as far as the Thousands Islands, a group of islets commonly
known as Kepulauan Seribu (van der Meij et al., 2009; Willoughby,
1986; Willoughby et al., 1997). Among the litter brought by the rivers,
polystyrene blocks, plastic bags, and discarded footwear are commonly
seen on the shorelines of Thousands Islands (Willoughby, 1986; Wil­
loughby et al., 1997).
Plastic litter is a global concern not only because it pollutes the ocean
and beaches, but also because it is ingested by aquatic birds, causes
entanglement and may be incorporated into nests (Azzarello and Van
Vleet, 1987; Battisti et al., 2019; Gil-Delgado et al., 2017). Bird fecal
matter contaminated with plastic particles has been observed in several
studies (Gil-Delgado et al., 2017). Five seabird families, Gaviidae, Dio­
medeidae, Sulidae, Stercoraridae and Alcidae, have been recorded as
having high interactions with marine litter (Battisti et al., 2019).
Although ingestion does not necessarily directly lead to death, plastic
litter can be stuck in the throat and swallowed, and chemicals such as
heavy metals contained in the litter can cause poisoning, which can lead
to death (Butterworth et al., 2012; Hong et al., 2013).
While the increasing quantities of litter in the ocean impact seabirds,
there is also increasing depositions of litter on the shoreline impacting
wildlife associated with coastal habitats, such as the shorebirds and
waders. In coastal ecosystems, mangroves play an important role in
providing habitat for wildlife, particularly waterbirds (Nagelkerken
et al., 2008). Waterbirds use mangroves for foraging, roosting, and
nesting sites (Mancini et al., 2018; McFadden et al., 2016), regulating
fish populations in mangroves (Miranda and Collazo, 1997). Mangroves
are also stopover sites for migratory waterbirds (Aarif and Prasadan,
2014; Crossland et al., 2006; Sandilyan and Kathiresan, 2015).
Mangroves are among the most productive ecosystem along the
coastline in the tropics and subtropics as they provide unique ecosystem
services and goods such as nursery grounds for fishes and shrimps, food
and habitat for many waterbirds and food, fuel, medicine and building
materials for local communities (Alongi, 2002; Giri et al., 2011).
Although covering only 0.1% of the earth’s surface, mangroves
sequester approximately 22.8 million metric tons of carbon each year
(Giri et al., 2011) and play important roles as coastline stabilizers
helping to protect the land from erosion (Alongi, 2002; Pham and
Yoshino, 2016). However, mangroves are usually sacrificed for devel­
opment in many large cities such as in Singapore, Hongkong, and Macau
(Glaser et al., 1991), as well as in Indonesia. The rate of mangrove loss in
Indonesia was approximately 100,000 ha/year from 2006 to 2012
(Ilman et al., 2016). Positioned in the frontline of the coast, mangroves
are exposed to anthropogenic disturbance such as the construction of
ponds and human settlements. Increased human populations is associ­
ated with increased litter in mangroves as they are usually located in
estuaries, which accumulate litter from the rivers (Alongi, 2002).
Several coastal plants such as Arundo donax, Carpobrotus spp., as well
as different mangroves species, are known to be barriers to litter
transport (Battisti et al., 2020; Cresta and Battisti, 2021; do Sul et al.,
2014; Gallitelli et al., 2021; Martin et al., 2019). Density of plants and
their structure may have a role in trapping litter. For example, the
tridimensional structure of Carpobrotus spp. retains different types of
litter (Gallitelli et al., 2021) while the aerial roots of mangroves trap
objects such as plastics that are easily retained and thus, not release
directly into the ocean (do Sul et al., 2014; Vieira et al., 2013). While
they have the important function of filtering pollutants, mangroves
covered in litter will have negative effects on the mangrove trees
2
Ocean and Coastal Management 225 (2022) 106223
themselves as well as the wildlife living in mangroves including
waterbirds.
Waterbirds are birds that depend on aquatic ecosystems for most of
their activities such as foraging, nesting, resting, and moulting. Most
waterbirds are either permanent residents of mangroves, or regular
visitors, daily or migrating seasonally (Ewel et al., 1998; Mancini et al.,
2018; Rajpar and Zakaria, 2014). Migratory birds travel long distances
and generally avoid polluted environments due to their high sensitivity
(Schreiber and Burger, 2001). Therefore, migratory waterbirds have
been used as bio-indicators (Caro and O’Doherty, 1999). The Index of
Marsh Bird Community Integrity (IMBCI) and the Index of Waterbird
Community Integrity (IWCI) (DeLuca et al., 2004, 2008) both use the
bird community to evaluate whether human disturbances in coastal
areas affect estuarine ecosystems. The IWCI, which uses waterbirds as
indicators, can evaluate the level of urbanization by recording the
waterbird community at a given location (DeLuca et al., 2008; Prosser
et al., 2017). This index can also assess the impact of other stressors on
the waterbird community (DeLuca et al., 2008).
From the land to the coast, litter has become a common part of the
environment for birds. Despite the extent of research on the impact of
litter on birds reviewed above, there is little available research on how
many birds are actually living with litter in mangroves. Therefore, in this
study, we evaluated how many birds are living closely with litter in the
coastal mangrove areas of Jakarta Bay. We also determined the distri­
bution and type of litter in the mangroves and the association of birds
with the type of litter. Finally, we calculated the Index of Waterbird
Community Integrity (IWCI) of the study areas to understand the im­
plications of litter as a stressor on bird communities in Indonesia. Such
results will provide baseline data to assess management
recommendations.
2. Materials and methods
2.1. Study area
We carried out our study at three sites (Fig. 1), mostly covered by
mangroves, along Jakarta Bay, and in proximity to residential areas: (i)
Arboretum Muara Angke (AMA); (ii) Angke-Kapuk Protection Forest,
(Hutan Lindung Angke-Kapuk, HLAK); and (iii) Angke-Kapuk Nature
Recreation Park (Taman Wisata Alam Angke-Kapuk, TWAAK) during
October–November 2020. Jakarta Bay extends between two capes,
Tanjung Pasir to the west and Tanjung Karawang to the east. HLAK is a
44.76 ha area managed by the Jakarta provincial government located
between the mouths of two rivers, Kamal and Angke (Sasongko et al.,
2014). The TWAAK of 99.82 ha is located in front of AMA, closer to the
sea. AMA of 10.52 ha is the smallest area with the least mangrove cover
(5.36 ha) (Putra, 2019), farthest from the coastline (Fig. 1). The three
sites, particularly TWAAK, are also used for recreation, especially by
local tourists. The mangrove community is dominated by Avicennia
marina (Avicenniaceae), Rhizophora mucronata, Rhizophora stylosa
(Rhizoporaceae), Sonneratia caseolaris (Sonneratiaceae), and Excoecaria
agallocha (Euphorbiaceae) (Sasongko et al., 2014).
2.2. Data collection
We used the point count method following Bibby et al. (2000) to
record the birds. Observers stand at a point and record each species and
the number of individuals of each species, seen or heard for a period of
10 min (Bibby et al., 2000). Observation points were spread along
existing paths. The distance between observation points was 150–200 m,
and each point was repeated at least twice. The number of points was
roughly proportional to the area. (Fig. 1). At each point, we also
measured salinity and canopy closure in 4 different directions. Salinity
was measured using a salinity refractometer. Canopy closure was
measured using Canopeo applications, which were then averaged (Pat­
rignani and Ochsner, 2015).
N.L. Winarni et al. Ocean and Coastal Management 225 (2022) 106223

Fig. 1. Location of the three study areas in Jakarta Bay, Arboretum Muara Angke (AMA), Hutan Lindung/Protected Forest (HLAK), Conservation Area (TWAAK) with
distributions of observation points.

At each point, we collected data on litter type and abundance of litter Community Integrity (IMBCI), with several developments that refer
using a modification of the method described by Lippiatt et al. (2013) for more to the natural history of water birds such as foraging niche
the NOAA Marine Debris Program. We used a circular sampling area breadth, migratory range, nesting site, breeding range, conservation
around the bird count point count with a 10 m radius. The NOAA marine status and native status (DeLuca et al., 2004, 2008; Prosser et al., 2017).
debris assessment method is a data collection technique that focuses on The equations are as follows:
calculating the amount and type of litter without removing litter (Lip­ ∑
piatt et al., 2013). In this study, we focused on small (≤30 cm) and large SIWCI = LS
(>30 cm) debris items with a minimum litter size of 2.5 cm. Large litter [ ∑ ]
(>30 cm) was recorded separately from small litter by recording the TIWCI =
SIWCI
+ 2(Ai )
type of litter as well as the status of litter (buried/submerged/stranded). SN
Small litter (≤30 cm) was categorized based on its main constituent
where Ls is the cumulative score of species attributes, SIWCI is species
materials, i.e., plastics, metals, glass, rubber, processed wood, or fabrics.
score, SN is the total number of species present at point, Ai is abundance
We also defined the plastic fragments recorded such as straws, plastic
score at each point, TIWCI is the score for each point. The cumulative
bottles, etc. The litter category was based on visual observation with
score of species attributes (Ls) was estimated on a scale of 1–4 in which
binoculars to aid the identification, as well as olfactory, or tactile ob­
the score attributes were modified to adjust to regional conditions in
servations. Concentration of each type of litter at each point was then
Indonesia. Species attributes included foraging niche breadth, nesting
calculated in units of #items/m2 (Lippiatt et al., 2013).
site selectivity, migratory range, breeding range, conservation status,
and native status. We modified the breeding range and conservation
2.3. Analysis
status where the breeding range comprised of Global, Asia, Southeast
Asia, and Indonesia, and the conservation status follows IUCN (Table 1).
We transformed litter concentration into log10 prior to analysis. We
The SIWCI ranged from 5 to 21. Birds with SIWCI > 10 are considered
then carried out linear regressions to determine the relationship be­
sensitive (S) and those with SIWCI < 10 are considered disturbance
tween number of species present at each point and litter, as well as
tolerant (DT). The rest of the analysis followed DeLuca et al. (2008).
number of waterbird species present at each point and litter. For this
TIWCI is the IWCI value at each point while EIWCI is the average result of
analysis, we only included birds which at least occasionally use the
the TIWCI value at each point (DeLuca et al., 2008). We did not calculate
ground or water which was usually covered with litter.
TIWCI if there were none or only one species present at a point.
We then calculated the Index of Waterbird Community Integrity
(IWCI) described by DeLuca et al. (2008), in which the presence and
abundance of waterbirds is used as a basis for assessing environmental
quality and the impact of anthropogenic disturbances. The definition of
waterbirds adopted by this index is all species that forage on aquatic
organisms. The index builds on the previous Index of Marsh Bird

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N.L. Winarni et al. Ocean and Coastal Management 225 (2022) 106223

Table 1 while 24 species were recorded in TWAAK (Table 2). Of these, 13 species
Modification of species score attributes for IWCI. were waterbirds. We noted the presence of the Near-threatened Sunda
Species Score teal (Anas gibberifrons) in all three study sites and the Endangered Milky
Attributes stork (Mycteria cinerea) in AMA and TWAAK (BirdLife International
Generalist Specialist
2022 IUCN Red List for birds. Downloaded from http://www.birdlife.
1 2 2.5 3 4 org on 17/05/2022) . We also noted the presence of the Indonesian
Foraging Habitat Aquatic Moderate Specialist honeyeater (Lichmera limbata) in TWAAK, which was potentially intro­
Niche Generalist Generalist Specialist duced as the species is originally found in Bali and the Lesser Sundas but
Breadth
is commonly sold in bird markets (Balen et al., 2015). The most common
Nesting Site Generalist Moderate Specialist
Selectivity Generalist waterbirds in all study areas were Javan pond heron (Ardeola speciosa),
Migratory Non- Short Medium Long Sunda teal (A. gibberifrons), and striated heron (Butorides striatus)
Range Migratory Distance Distance Distance (Table 2). AMA, which is located inland, presented a considerably open
Breeding Global Asia Southeast Indonesia canopy, while the other two areas positioned along the coastline had
Range Asia
Conservation Least Near Vulnerable Endangered
more closed canopies (HLAK, 13.64 ± SE 2.57; TWAAK
Status Concern Threatened (11.19 ±SE 7.53). AMA has also the highest salinity followed by
Native Status Non- Native TWAAK and HLAK (Table 2).
nativea
a
Non-native is regarded as 0. 3.2. Litter composition and correlations with birds

3. Results
3.1. Bird community and the mangrove habitat
In total, we recorded 34 bird species at 32 observation points in the
three study areas. There were 23 species recorded in AMA and HLAK,
Plastic (89%) was the most abundant type of litter in the study area,
followed by processed wood litter (6%), then rubber and fabric litter, 2%
and 1.9% respectively. Metal, and glass comprised less than 1%. HLAK
contained more litter than TWAAK (Table 3). The highest concentration
of litter was found at the observation point HL01 (5.41 items/m2) which
was positioned on the coastline, followed by point TWA02 (2.24 items/

Table 2
Bird encounter rates at the three study sites (asterisks designate waterbirds) and their presence at litter points, with number of points surveyed, bird species and
waterbird species richness, as well as EIWCI.
Species English Name AMA HLAK TWAAK Present at litter point

Acridotheres javanicus Javan myna 0.14

Actitis hypoleucos * Common sandpiper 0.09 0.52 0.29 yes
Aegithina tiphia Common iora 0.38 yes
Alcedo coerulescens * Cerulean kingfisher 0.14 0.33 yes
Amaurornis phoenicurus * White-breasted waterhen 0.23 0.19 yes
Anas gibberifrons * Sunda teal 0.68 2.86 0.58 yes
Anhinga melanogaster * Oriental darter 0.05 0.04
Anthreptes malacensis Brown-throated sunbird 0.14 0.10 0.04 yes
Ardea purpurea * Purple heron 0.04 yes
Ardeola speciosa * Javan pond heron 1.23 0.62 0.50 yes
Artamus leucorynchus White-breasted woodswallow 0.05 yes
Butorides striatus * Striated heron 0.55 0.57 0.71 yes
Cinnyris jugularis Olive backed sunbird 0.23 0.08 yes
Crypsirina temia Racked-tailed treepie 0.21 yes
Dendrocopos macei Fulvous-breasted woodpecker 0.09 0.10 yes
Dendrocopos moluccensis Sunda pygmy woodpecker 0.14 0.14 yes
Dicaeum trochileum Scarlet-headed flowerpecker 0.38 0.13 yes
Egretta garzetta * Little heron 0.14 0.19 0.29 yes
Geopelia striata Zebra dove 0.04
Gerygone sulphurea Golden-bellied gerygone 1.41 0.19 1.00 yes
Lichmera limbata Indonesian honeyeater 0.08 yes
Lonchura leucogastroides Javan munia 0.73 0.14 0.13 yes
Lonchura punctulata Scaly-breasted munia 0.50
Mycteria cinerea * Milky stork 0.05 0.08
Nycticorax nycticorax * Black-crowned night heron 0.04
Orthotomus ruficeps Ashy tailorbird 0.14 0.14 0.04 yes
Orthotomus sutorius Common tailorbird 0.05 0.14 0.46 yes
Passer montanus Eurasian treesparrow 0.52 yes
Phalacrocorax sulcirostris * Little black cormorants 0.19 0.04 yes
Pycnonotus aurigaster Sooty-headed bulbul 0.32 0.90 yes
Pycnonotus goiavier Yellow-vented bulbul 0.32 0.33 0.29 yes
Rhipidura javanica Sunda pied fantail 0.14 0.24 0.21 yes
Spilopelia chinensis Spotted dove 0.27 0.33 0.13 yes
Todiramphus chloris * Collared kingfisher 0.10 yes

Number of species 23 23 24 28
Waterbird species 9 8 11 10
Number of points 11 7 14
Canopy cover 0% 13.64% 11.19%
Salinity 15.29 21.14 22.82
EIWCI 15.66 14.64 15.26

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N.L. Winarni et al. Ocean and Coastal Management 225 (2022) 106223

Table 3 3.3. Index of waterbird community integrity (IWCI)

Litter concentration composition in HLAK and TWAAK.
Litter types HLAK TWAAK Total Among the 34 bird species, 13 species were waterbirds. TWAAK had
the largest number of waterbird species compared to AMA and HLAK
Overall 63% 37% 99.9%
Plastic 89.0% 90.4% (Table 1). The IWCI was highest in AMA, followed by TWAAK and HLAK
Metal 0.7% 0.4% although they were not much different. The score for species (SIWCI)
Glass 0.5% 0.4% varied from 9 to 18, with M. cinerea showing the highest sensitivity
Rubber 2.0% 1.2% score, followed by Anhinga melanogaster and Alcedo coerulescens. Only
Processed wood 6.0% 7.5%
Fabrics 1.9% 0.2%
two species were disturbance tolerant, Ardeola speciosa and Butorides
Litter size striatus (Table 4). The IWCI at different points in AMA, HLAK, and
Small (≤30 cm) 94% 96% 94.5% TWAAK ranged between 12 and 17 (Table 5). The number of waterbird
Large (>30 cm) 6% 4% 5.5% species present at points showed a positive relationship to the TIWCI (R2
Status of large litter
= 0.443, P < 0.001) (Fig. 6). When looking at the relationship between
Buried 3.8% 0 2.7%
Stranded 96.2% 100% 97.3% IWCI at points, we found that IWCI tended to be low when there was
more litter although the relationship was not significant (R2 = 0.003, P
= 0.82). However, patterns in the abundance of litter matched the IWCI.
m2) and point HL04 (2.06 items/m2). At these points, concentrations of AMA, with the highest IWCI, had no litter, followed by TWAAK, and
different types of litter were higher, particularly plastics, processed HLAK.
wood, and rubber. Only 4 points at TWAAK (TWA05, TWA07-08,
TWA13) were litter free (Fig. 2). Interestingly, all observation points 4. Discussions
at AMA were litter free.
In HLAK and TWAAK, most plastic litter was in the form of frag­ 4.1. Litter and bird communities in mangroves
ments, cups, food wrappers, plastic bags, plastic bottles, and bottle caps
(Figs. 2 and 3). Most processed wood litter was logs, while rubber litter Although mangroves are considered to be among the most produc­
was mostly in the form of flip-flops and fragments. Overall, there was tive ecosystems, it is a double-edged sword because mangroves also tend
more small litter (94.5%) than large litter (5.5%). Among the large litter, to accumulate more litter. Inundation at high tide transports litter ma­
2.7% was buried, and 97.3% was stranded (Table 3). HLAK and TWAAK terial to the ocean (Martin et al., 2019), and most of the litter is trapped
retained similar litter but there was no buried litter found in TWAAK among the roots of mangroves. Different locations in mangrove forests
(Table 3). Representative pictures of AMA, HLAK, and TWAAK are also affect the retention of litter, with the higher grounds and areas of
presented in Fig. 4. dense trees tending to trap more litter objects (do Sul et al., 2014). Some
There were 28 bird species present at points with litter (Table 2). of our observation points retained more litter than others, not just
However, only 21 species including waterbirds and ground foraging plastics but also other materials such as processed wood and fabrics. The
birds, were used to analyse the relationship between birds and litter litter-free Arboretum (AMA), which is located inland, has sparser trees
because we assumed that the seven canopy bird species have no direct and less mangrove cover than the other two areas, which explains the
encounter with litter. We found that there was no relationship between zero litter (Putra, 2019). Inland basin mangroves tend to have less
the total number of birds (R2 = 0.004, P = 0.78) or number of waterbirds plastic litter than coastal fringe mangroves (van Bijsterveldt et al.,
(R2 = 0.038, P = 0.40) and litter concentration. Three waterbird species, 2021). Various types of litter were found in HLAK and TWAAK, where
Oriental darter (A. melanogaster), Milky stork (M. cinerea), and Black- there were smaller litter particles than large particles and more stranded
crowned night heron (N. nycticorax) were never present where there litter than buried.
was litter (Table 2). The Spearman correlation test suggested that there Plastics such as food wrappers, cups, plastic bags, and straws can
were birds that correlated positively or negatively with litter (Fig. 5). break into fragments, which made up most of the plastic litter in the
There were 18 species which showed negative correlations with litter, HLAK and TWAAK. Similar situations were also observed in Pulau
and amongst them, only 8 species showed significant negative correla­ Rambut, an island within the Thousands Islands, approximately 30 km
tions. These were Javan myna (Acridotheres javanicus), Oriental darter away from Jakarta. Litter drifting away from Java ended up in islets such
(Anhinga melanogaster), Little egret (Egretta garzetta), Javan munia as Pulau Rambut where 14 waterbird species depend on the mangrove
(Lonchura leucogastroides), Scaly-breasted munia (L. punctulata), Milky habitat for nesting (Firdausy et al., 2021; Nadyanti, 2020). There was
stork (Mycteria cinerea), Yellow-vented bulbul (Pycnonotus goiavier), and also evidence of litter present in waterbird and seabird nests (Firdausy
Spotted dove (Spilopelia chinensis). None of the birds were positively et al., 2021; Massetti et al., 2021). Taking a long time to degrade,
correlated with litter (Fig. 5). plastics can be detrimental to mangroves because of the risk of pro­
longed suffocation of pneumatophores, inhibiting growth and causing

Fig. 2. Distribution and concentration of litter in observation points at HLAK and TWAAK.

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N.L. Winarni et al. Ocean and Coastal Management 225 (2022) 106223

Fig. 3. Types of 5 most abundant plastic litter in the overall study areas.

Fig. 4. Representative pictures of AMA, HLAK, and TWAAK.

Fig. 5. Spearman correlation between bird species and litter (numbers in bold show the significant correlations).

leaf loss (van Bijsterveldt et al., 2021). Over time, plastic litter breaks Although there were no relationships between litter and overall
down into microplastics of sizes <5 mm. This small size makes it easier species richness, litter depositions may affect different bird species.
for microplastics to enter the food chain and accumulate in the body of Among the 21 bird species which use water and the ground below
organisms (van Raamsdonk et al., 2020). mangroves, 38% correlated negatively with the concentration of litter

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N.L. Winarni et al. Ocean and Coastal Management 225 (2022) 106223

Table 4 Birds may forage at litter dumps and the presence of litter increases
List of waterbirds with species score (SIWCI) and sensitivity (S = sensitive, DT = the risk of pathogenic infection when there is direct contact between
disturbance tolerant). birds and litter (Plaza et al., 2019). Pathogen infection can cause various
Species name SIWCI Sensitivity diseases and even death. The ability to move between habitats is also
Actitis hypoleucos 10.5 S
likely to transmit pathogenic infections (Navarro et al., 2019). Birds
Alcedo coerulescens 13.5 S such as Milky stork tend to forage in mangroves but also range inland to
Amaurornis phoenicurus 10 S fishing ponds and even rice fields along the east coast of West Java.
Anas gibberifrons 12.5 S Feeding on small fish of the coastal and brackish water, and sometimes
Anhinga melanogaster 13.5 S
also feeding on snakes and frogs, these bird feed opportunistically by
Ardea purpurea 11 S
Ardeola speciosa 9 DT probing the mudflats (Urfi, 2011; Verheugt, 1987), which increases
Butorides striatus 9.5 DT direct contact with buried and stranded litter.
Egretta garzetta 10.5 S Aside from the risk of pathogenic infection, birds foraging in areas
Mycteria cinerea 18 S with a lot of trash are at risk of accidently ingesting litter. Many records
Nycticorax nycticorax 10 S
Phalacrocorax sulcirostris 11.5 S
of seabirds have been found with litter in their digestive tracts because
Todiramphus chloris 10 S they mistook it for food as it had a shape or smell similar to food (Cadée,
2002; Derraik, 2002; Savoca et al., 2016; Wabnitz and Nichols, 2010).
Swallowed litter can obstruct the digestive tract, injure internal organs,
including the Endangered Milky stork, Oriental darter, and Little egret result in heavy metal poisoning, cause reproductive disorders, and even
suggesting that certain species are more susceptible to being impacted mortality (Butterworth et al., 2012; Gilbert et al., 2016; Roman et al.,
by litter (Hong et al., 2013). 2019; Van Franeker and Law, 2015). Another threat to birds from ma­
Following Battisti et al. (2019), the correlations with litter may rine debris is entanglement. Accidents of entanglement by marine debris
indicate that there are interactions between birds and litter. Further are becoming more frequent and more dangerous than cases of litter
research is needed to explain such interactions. These results, however,
are additions to the list of birds interacting with litter (Battisti et al.,
2019). The little egret has been reported to have become entangled with
litter (Hong et al., 2013). The Milky stork and Oriental darter were never
present where there was litter. Feeding or foraging patterns, body size
and shape, as well as behaviour may be factors influencing the suscep­
tibility of birds to litter (Hong et al., 2013). Large-sized pursuit diving
birds (plunging from a height while searching for surface prey) such as
Oriental darter can accidently swallow litter during hunting (Tavares
et al., 2017) and tactile surface hunters like Milky stork will tend to be
more affected by litter as they move and probe alternatingly to search
for prey (Anugra et al., 2021). These birds preyed on both slow and
fast-moving benthic fishes (Narayanan and Thomas, 2016), and there­
fore avoid areas with litter as it can obscure their view. Although they
avoid litter, there have been reports of heavy metals such Pb and Cd
contaminating the Milky stork’s habitat and affecting the fishes and
shrimps, which are their food source (Ismail et al., 2011; Rahman et al.,
2017). In addition, there are birds other than waterbirds that use man­
groves as foraging and nesting habitat such as the Javan myna (Acri­
dotheres javanicus), Yellow-vented bulbuls (Pycnonotus goiavier), and
Spotted dove (Spilophelia chinensis), birds which are common in urban
areas (Mardiastuti et al., 2020; Winarni et al., 2021). These species were
also negatively correlated with litter. This shows that this type of litter Fig. 6. Line fit plot between TIWCI and number of waterbird species present at
also affects highly adaptive birds such as urban birds. each point.

Table 5
TIWCI and number of waterbird species at each observation point, as well as overall EIWCI in the three study areas.
AMA HLAK TWAAK

Points IWCI No. Waterbirds Points IWCI No. Waterbirds Points IWCI No. Waterbirds

AR 01 16.38 4 HL01 1 TWA 01 15.00 4

AR 02 14.30 5 HL02 16.30 5 TWA 02 15.83 3
AR 03 15.75 4 HL03 14.83 6 TWA 03 15.67 3
AR 04 17.00 3 HL04 12.00 2 TWA 04 12.00 3
AR 05 13.88 4 HL05 14.25 4 TWA 05 14.25 2
AR 06 11.50 2 HL06 17.00 3 TWA 06 1
AR 07 16.25 2 HL07 13.50 1 TWA 07 15.60 5
AR 08 17.25 2 TWA 08 15.29 7
AR 09 0 TWA 09 1
AR 10 16.67 3 TWA 10 0
AR 11 17.67 3 TWA 11 16.63 4
TWA 12 1
TWA 13 16.00 2
TWA 14 16.33 3

EIWCI 15.66 14.65 15.26

7
N.L. Winarni et al.
ingestion (CBD, 2012). Birds caught in entanglements will get injured,
run out of energy when they try to escape from the snare, be unable to
hunt properly, and might even die (Bertram et al., 2021; Laist, 1997;
Putz and Hiriart Bertrand, 2011).
4.2. IWCI as an indicator of healthy mangroves
The distribution of remaining mangroves around Jakarta Bay is
limited and usually confined to narrow areas, which may be leading to
low waterbird species richness. There was slightly higher species rich­
ness in TWAAK than in AMA and HLAK. However, AMA and TWAAK
have slightly better IWCI than HLAK, which is likely due to the number
of waterbird species present at bird count points. AMA and TWAAK also
have rare and migratory waterbirds such as Milky stork (Kristanto and
Iqbal, 2013). Birds, including waterbirds play a role as indicators of
changes in the environment (Carignan and Villard, 2002; Ogden et al.,
2014; Winarni and Jones, 2012). Waterbirds are important indicators of
healthy coastal habitat due to their sensitivity to changes in the envi­
ronment (Ogden et al., 2014). Seabirds and waterbirds are also potential
indicators of the distribution and types of plastic litter, when they are
ingested (Coughlan et al., 2020; Ryan et al., 2009). In the overall study
area, the highest species score was the Milky stork, which scored 18.
This species has the longest migratory range compared to other species
recorded. Located in Jakarta Bay, which is subjected to high anthropo­
genic disturbance, the study area was less likely preferred as a migratory
stopover site for most species.
IWCI was applied to shoreline and sub-estuary locations in Ches­
apeake Bay, US, and 42% of the waterbirds recorded had a species score
>15 (Prosser et al., 2017). IWCI has never been applied to mangroves
before. In our study, only milky stork had a score >15. Moreover, only
two species, Javan pond heron (Ardeola speciosa) and striated heron
(Butorides striatus), were disturbance tolerant. Javan pond heron was an
abundant species at a sewage treatment (Dalem et al., 2011) and other
research has found low concentrations of Cr, Cu, Ni, Pb, and Hg in the
body tissue of striated heron, suggesting that these two birds may be
able to cope with long-term exposure to heavy metals (Simonetti et al.,
2014).
IWCI incorporates anthropological changes in the environment
including development of infrastructure and changes to landcover
(DeLuca et al., 2008; Prosser et al., 2017, 2018). Litter, however, is not
directly related to landcover nor infrastructure changes. Although not
significant, patterns of IWCI at the three study areas were consistent
with patterns of litter concentration; more litter corresponded to a
decrease in the IWCI. Waterbirds responded to the drivers of environ­
mental disturbance involving litter (Ogden et al., 2014), and therefore
are potential indicators of litter concentration in coastal habitats
including mangroves. Continuous monitoring should be carried out
regularly and the decreasing values of IWCI should be used as an alarm
for an improvement in the management.
4.3. Litter management in mangroves
There are two different mangrove types in Jakarta Bay based on
hydrological conditions. HLAK and TWAAK are fringe mangroves and
AMA is basin mangroves, which should be taken into account in con­
servation management (Ewel et al., 1998; Lugo and Snedaker, 1974;
Nugroho et al., 2019). HLAK and TWAAK have more mangrove cover
with the aerial roots tend to retain plastic litter. Fringe mangroves occur
on the coastline exposed to the open sea and are an important safeguard
against abrasion by maintaining the shape and structure of the coast
(Herison et al., 2014). However, this function is not working effectively
when the mangroves are covered with litter or replaced by other
waterfront infrastructure (Herison et al., 2014; Martin et al., 2020).
Reclamations on the waterfront have added stones, breakwaters and
fences, which cause litter to pile up, potentially creating a long-term sink
for plastic litter generating harm to waterbirds (Herison et al., 2014).
8
Ocean and Coastal Management 225 (2022) 106223
The mangroves along the coast of Jakarta Bay were mostly composed
of Avicennia marina, which was often planted during restoration pro­
grams and for the protection of the coastline against erosion (Herison
et al., 2014). However, stranded plastics may suffocate the aerial roots,
the pneumatophores, of these trees and may cause death of the
mangrove trees. van Bijsterveldt et al. (2021) suggested that plastics
tend to be buried in the upper layer of sediment which may halt the
growth of mangrove seedlings. A restoration program, therefore, should
also plan for mitigating threats such as litter by including the removal or
prevention of litter to avoid prolonged suffocation of roots (van Bij­
sterveldt et al., 2021).
Litter dynamics in the mangroves are likely related to the magnitude
of tidal inundation (Twilley et al., 1986). Basin mangroves such as AMA,
which are located inland behind fringe coastal mangroves, tend to have
stagnant water and lower tidal activity. Compared to fringe mangroves,
basin mangroves were less preferred as a stopover by migrating birds,
possibly because there are fewer food resources than in the frequently
inundated areas of fringe mangroves (Ewel et al., 1998). However,
inland mangroves tend to retain less litter than fringe mangroves (van
Bijsterveldt et al., 2021). Therefore, remedial activities should concen­
trate in fringe mangroves.
Birds such as the endangered Milky stork are suffering an alarming
population decrease (Iqbal et al., 2012; Verheugt, 1987). The negative
correlation with litter suggests that these birds are sensitive to anthro­
pogenic disturbance and will avoid areas covered with litter. Litter,
therefore, must be removed or prevented from accumulating in the first
place to accommodate better habitat for the Milky stork. With the closest
breeding sites in Pulau Rambut (Verheugt, 1987), the polluted envi­
ronment on the coastline of Jakarta Bay will contribute to the decrease
of the remaining population. AMA and TWAAK were potentially better
for waterbirds, as shown by the IWCI which shows that more waterbird
species were present in the two areas. Given the conditions in the three
study areas, adoption of the following points by management may lead
to better habitats for biodiversity:
• Adjust management so to take account of different mangrove types
based on hydrological conditions. Control of litter should be focused
on fringe mangroves, which tend to trap litter.
• Restoration of mangroves should include plans to mitigate the effects
of litter by removing it, including buried litter
• Better control of human activities including tourism and other en­
terprises within river catchments to reduce litter dumping
• Milky stork and other species which are negatively correlated with
litter can be used indicators of litter concentration by monitoring
their abundance and distributions
4.4. Policy and conservation management of mangroves
Indonesia has been a member of the Conventions on Wetlands of
International Importance, Especially as Waterfowl Habitat, known as
Ramsar Convention since August 8, 1992. The obligation of parties to
this convention is to maintain their wetlands and specifically to protect
the wetlands that have international importance included in a pre­
determined list convention (Anggara, 2018). Wetlands are marshes,
peatland, or areas inundated by water permanent or temporarily,
brackish or salt, i.e., beaches, estuaries, mangroves, etc. (Scott and
Jones, 1995). Management of Ramsar sites includes restorations of
degraded wetlands habitats, habitat management, protection from in­
vasion by alien species, regulation on the use of natural resources,
management of stakeholders and their activities, and development of
supporting infrastructure such as wetland education centers. The
designation of Ramsar sites is known to have significant impact on
waterbird species richness and abundance (Kleijn et al., 2014; Popoff
et al., 2021). There are seven Ramsar sites in Indonesia. The only one
close to Muara Angke is Pulau Rambut. Muara Angke areas have been
designated as an Important Bird Areas by the NGO BirdLife International
N.L. Winarni et al.
(IBA) (Chan et al., 2004; Rudyanto and Rombang, 1999). The protection
of Muara Angke may support the protection of the Pulau Rambut Ramsar
site through the role it plays in the East Asian – Australasian Flyway
(EAAF), one of the major migratory bird routes that crosses the Sou
(MacKinnon et al., 2012) theast Asian countries (MacKinnon et al.,
2012) because Muara Angke provides foraging sites for birds from Pulau
Rambut as well as other migratory birds. Muara Angke and the Jakarta
Bay areas are included in this EAAF (Tirtaningtyas & Yordan, 2017)
because of their importance to the overall flyway of birds to and from
Australia each year. Pollution including litter is considered to be the
greatest threat to the wetland habitats of the EAAF (MacKinnon et al.,
2012).
The remaining mangroves around Jakarta Bay are confined to nar­
row areas. Mangrove areas in Jakarta have been replaced by de­
velopments particularly for housing and business districts. Mangroves
receive additional threats from developments because of the associated
litter dumping into adjacent coastal waterways (Alongi, 2002). In
addition, there are also reclamation projects on the waterfront of Jakarta
Bay. In effect, the ecological functions of mangroves are being degraded
(Slamet et al., 2020).
The Government of Indonesia formed the National Action Plan for
Marine Debris Management 2018–2025 through Presidential Regulation
No. 83 of 2018 (Purba et al., 2019). There are five strategies, which
cover (1) national awareness program for stakeholders, (2) litter man­
agement sourced from land-based activities, (3) litter management on
coastal and sea areas including management of plastic litter, (4) funding
mechanisms, institutional strengthening, supervision, law enforcement,
and (5) research and development (Lumbanraja et al., 2020). However,
there are no specific actions aimed at mangroves or Ramsar sites. Posi­
tioned in low-lying densely populated areas, wetland habitats such as
Muara Angke may be less attractive to conservationists than terrestrial
forest habitats with are rich in endangered megafauna (Yong et al.,
2022). However, they may be important to support waterbird breeding
areas and nearby Ramsar sites such as Pulau Rambut.
Therefore, there is a need for the Ramsar management activities and
marine debris management to be integrated. There is also an opportu­
nity to explore the use of waterbirds as indicators of the environmental
health of mangroves, which might then be mainstreamed into major
policy frameworks and initiatives. The IWCI index by indicating
waterbird species richness and abundance is a simple method which can
be used to monitor mangrove areas regularly to assess whether man­
agement measures are succeeding.
5. Conclusions
In this study, the impacts of litter on birds, which includes waterbirds
and all other birds that use the ground within the mangroves of Jakarta
Bay were elucidated. All birds were affected to some extent by the
presence of litter in the mangroves. Fringe mangroves tend to retain
more litter, which consisted mostly of plastics. Birds such as the En­
dangered Milky stork and Oriental darter were never present where
there was litter. The Index of Waterbird Community Integrity (IWCI)
was not statistically related to the presence of litter, although more litter
did reduce the IWCI. Management implications drawn from our results
suggested that regular monitoring of IWCI would be useful as an indi­
cator for successful management by considering the different types of
mangrove hydrological conditions, include plans of removing litter
during restoration programs, control of littering by human activities,
and regularly monitor the abundance of waterbirds that negatively
correlated to litter.
Author contributions
NLW and DHP were responsible for research design, synthesis, and
writing. SAA, NZ, YW, DS, BGA, were responsible for data collection and
analysis.
9
Ocean and Coastal Management 225 (2022) 106223
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This work was supported by the funding from Universitas Indonesia
Hibah PUTI Q2 (NKB-1659/UN2.RST/HKP.05.00/2020). We thank all
the staff of the Research Center for Climate Change-Universitas
Indonesia who supports and help us during research and analysis. We
also thank Chris Margules, Thasun Amarasinghe, and several anony­
mous reviewers for reviewing and shaping the manuscript. We followed
all applicable ethical guidelines and permits to conduct research
following regulations in Indonesia.
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