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to 1200 m offshore. Sediments were mostly muddy and contained substantial organic matter (typically .7%); waters were warm (,30uC) and somewhat brackish ( ...
Journal of Foraminiferal Research, v. 44, no. 2, p. 143–150, April 2014

BENTHIC FORAMINIFERAL DISTRIBUTIONS AS BIOINDICATORS IN COASTAL WATERS OF PENANG NATIONAL PARK, MALAYSIA FATIN I. MINHAT1,4, KHAIRUN YAHYA2, ANITA TALIB3 ABSTRACT

AND

OMAR AHMAD1

distribution is mainly affected by environmental factors in their microhabitat. The interplay among physical, chemical, and biological conditions allows certain species to thrive, while excluding others (Jorissen, 2003). Benthic foraminifera are used in many efforts to monitor biological, chemical, and thermal pollution (Alve, 1995). Their abundance, preservation potential, diversity, environmental tolerances, wide distribution, and cost effective sample collecting have made foraminifera excellent monitoring indicators (Alve, 1995; Scott et al., 2001; Murray, 2006). This study uses physical and chemical parameters together with foraminiferal assemblages and distributions to assess coastal waters and sediment quality around Penang National Park.

The distribution and abundance of benthic foraminifera were studied along the coastal waters of Penang National Park, Malaysia, at four sites (Teluk Bahang, Teluk Aling, Teluk Ketapang, and Pantai Acheh) representative of varying levels of anthropogenic activities. A total of 144 sediment and water samples was collected and environmental parameters measured bimonthly between October 2010–September 2011 along four transects at 200-m intervals from the low-tide line to 1200 m offshore. Sediments were mostly muddy and contained substantial organic matter (typically .7%); waters were warm (,30uC) and somewhat brackish (,29–30%). Specimens of the stress-tolerant genera Ammonia and Elphidium dominated assemblages along all transects. Cluster analysis separated the stations into four groups. The Group A1 stations (200 m offshore of Teluk Bahang and Teluk Aling) were characterized by the sandiest sediments, highest organic sediment concentrations (17%), a tendency for hypoxia [mean Ammonia-Elphidium Index (AEI) = 98], highest foraminiferal abundances (mean: 359 individuals/ cm3), and relatively low diversities (mean H9= 0.25). Group A2 included mostly Pantai Acheh stations, where mean concentration of organic matter (11%) and foraminiferal density (57 individuals/cm3) were lower than in Group A1 stations, diversity was slightly higher (H9= 0.37), and the AEI was similar (97). Group B1 represented the most stations from 11 sites in Teluk Bahang, Teluk Aling, and Teluk Ketapang, and had the lowest mean organics (9.7%) and intermediate densities (42 individuals/cm3) and diversities (H9= 0.45). Group B2 included only the Teluk Ketapang stations furthest from shore, with the lowest mean foraminiferal densities (7 individuals/cm3) and AEI (79) and the highest diversities (H9= 0.56). The Teluk Ketapang site was also the least subject to anthropogenic stressors. The spatial distributions of foraminifera appeared to reflect the sedimentary environment and input of labile organic matter from anthropogenic sources.

STUDY AREA The study was conducted in the coastal waters of Penang National Park, Penang Island, Malaysia (Fig. 1) at four sampling sites: Teluk Bahang, Teluk Aling, Teluk Ketapang, and Pantai Acheh. The depth ranged between 1.5– 10 m, with predominantly muddy substrate at most stations. These coastal waters are influenced by two prevailing seasons from the northeast and southwest (Chua et. al., 2000). The northeast one brings monsoon rain from December–February, while during the southwest season (June–August) the island experiences dry weather. Sampling sites were based on the nature of human activities present within the region. Inshore fishing and floating-cage aquaculture are major economic activities in Teluk Bahang. Teluk Aling is situated in a sheltered coastal area next to Teluk Bahang. The only human activities nearby are related to the Centre for Marine and Coastal Studies (CEMACS), Universiti Sains Malaysia. Teluk Ketapang is a sheltered bay situated 3 km southwest of Teluk Bahang. There is no development along its intertidal area, and therefore, it is considered a less disturbed site. Finally the Pantai Acheh sampling site is situated further south, closer to the mangrove ecosystem (Balik Pulau) of the Pinang River. Major anthropogenic activities occur near Pantai Acheh, as mangroves has been cleared for aquaculture ponds and housing, and thereby contribute to the effluent (domestic, aquaculture, and agriculture) discharge into the river (Nurul Ruhayu, 2011).

INTRODUCTION Benthic organisms, both macrofauna and meiofauna, have long been recognized as good bioindicators due to their limited movement, which can expose them to pollutants for prolonged periods. Benthic foraminifera are highly abundant meiofauna, sometimes making up 80% of the biomass (Snider et al., 1984), and are ubiquitous in nearly all marine environments (Sen Gupta, 2003). Their

MATERIALS AND METHODS One hundred forty-four sediment and water samples were collected bimonthly between October 2010 and September 2011. These samples together with in situ measurements of temperature, salinity, dissolved oxygen, and pH were obtained along a transect (Fig. 2) from the low-tide line to 1200 m offshore at 200-m intervals. Bulk sediments were collected using a 603 60 Ponar grab. These sediments were

1

Centre for Marine and Coastal Studies, Universiti Sains Malaysia, 11800, Penang, Malaysia 2 School of Biological Sciences, Universiti Sains Malaysia, 11800, Penang, Malaysia 3 School of Distance Education, Universiti Sains Malaysia, 11800 Penang, Malaysia 4 Correspondence author. E-mail: [email protected]

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FIGURE 1. Location of sampling sites offshore from Penang National Park, Malaysia: Teluk Bahang (05u47.19N, 100u20.89E), Teluk Aling (05u47.79N, 100u19.89E), Teluk Ketapang (05u39.69N, 100u15.89E), and Pantai Acheh (05u46.29N, 100u16.69E).

immediately subsampled using a hand corer with 5-cm inner diameter and transferred to 250-ml pre-labelled containers. Samples were then fixed with 4% buffered formalin to minimize foraminiferal test degradation (Hulings & Gray, 1971). Water samples from ,1 m above the seafloor were collected with a water sampler (Horizontal Transparent Acrylic 2.2 L), stored in 1-L polyethylene bottles, and taken to the laboratory for further analysis. From each preserved sediment sample, two 8-cm3 subsamples were taken randomly for quantitative analysis of foraminifera. The subsamples were wet-sieved using 1000mm and 63-mm sieves. The residue on the 63-mm sieve was carefully transferred into a 10-cm3 counting chamber using distilled water, and picked with a fine artist’s brush

(Somerfield et al., 2005). Counting and sorting were completed with the aid of a dissecting microscope (Meiji EMZ 57378). Total foraminiferal densities were based on sediment volume (cm3). Generic identification was based on Millet (1899), Cushman (1928), Loeblich & Tappan (1987), and Sen Gupta (2003). Selected samples were dried and photographed with a Carl Zeiss SMT scanning electron microscope. Several indices were calculated using the foraminiferal assemblage data, including the Shannon Diversity Index (H9) as described by Barbosa et al. (2009) and Narayan & Pandolfi (2010), the FoRAM Index of Hallock et al. (2003) as modified by Carnahan et al. (2009), and the AmmoniaElphidium Index (AEI) of Sen Gupta et al. (1996).

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FIGURE 2. Station locations at each sampling transect. PA 5 Pantai Acheh, TK 5 Teluk Ketapang, TA 5 Teluk Aling, TB 5 Teluk Bahang.

Sea-water samples were analyzed for nutrient content (nitrate, ammonium, nitrite, and phosphate) and total suspended solids, based on the methods of Strickland & Parsons (1972). Grain-size analysis followed the procedure of Bale & Kenny (2005). The loss on ignition (LOI) method was used to determine the percentages of organic matter in sediment (Bale & Kenny, 2005). Cluster analysis was carried out to interpret the response of foraminiferal assemblages to the environmental gradients (Murray, 2006). RESULTS Fourteen foraminiferal genera were identified in this study. The assemblage was dominated by Ammonia (56%), Elphidium (9%), and Ammobaculites (8%). Less abundant (,5%) genera included Astacolus (4.5%), Bolivina (3.5%), Quinqueloculina (3.4%), Nonion (3.3%), Reophax (2.8%), Textularia (2.6%), Fissurina (1.9%), Lagena (1.5%), Eggerella (1.5%), Hopkinsina (1%), and Asterorotalia (1%). Most genera were found at all sampling sites except for Hopkinsina that was not detected from Teluk Bahang and Teluk Ketapang, and Quinqueloculina, Lagena, and Asterorotalia that were absent at Teluk Bahang. The mean values for environmental parameters are given in Table 1. The average salinity recorded in Teluk Bahang (29.8 6 0.9%), Teluk Aling (29.6 6 0.5%), Teluk Ketapang

(29.6 6 0.5%) and Pantai Acheh (29.1 6 1.3%) throughout this study indicated coastal salinities typical of west peninsular Malaysia. Nutrient analysis showed the mean concentration of nitrite (NO2) at 0.15 6 0.0 mg/L, nitrate (NO3) at 0.01 6 0.0 mg/L, ammonia (NH4) at 0.02 6 0.00 mg/L, and phosphate (PO4) at 0.12 6 0.0 mg/L. These concentrations indicate that water quality at all sites could potentially fall into Class 2, according to the Malaysia Marine Water Quality Criteria and Standard (excerpted from the Malaysian Meteorological Department, 2010; Table 2). Organic matter was abundant in most sediment samples, ranging from ,3–34%. Concentrations of organic matter were generally higher closer to the shore (mean 16.4% 6 1.7 at 200 m; p , 0.05, Tukey’s test), decreasing significantly (mean 7.07% 6 0.41) at 800 m from shore toward the open sea. Figure 3 shows the distribution of organic matter along all transects throughout the sampling months. CLUSTER ANALYSIS The Q-mode hierarchical cluster analysis produced two major groups (A and B) with subgroups (A1, A2, B1, and B2; Fig. 4). Group A1 is comprised of samples from two stations located 200 m from shore in Teluk Bahang and Teluk Aling. This group has extremely high mean density (359 individuals/cm3) but low diversity (H95 0.25). Ammonia

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TABLE 1. Means and standard deviations for water and sediment parameters for all sampling stations at Teluk Bahang (TB), Teluk Aling (TA), Teluk Ketapang (TK), and Pantai Acheh (PA) between October 2010–September 2011.

Stations

Latitude

Longitude

Depth m

TB200 TB400 TB600 TB800 TB1000 TB1200 TA200 TA400 TA600 TA800 TA1000 TA1200 TK200 TK400 TK600 TK800 TK1000 TK1200 PA200 PA400 PA600 PA800 PA1000 PA1200

46.3789 46.7579 47.1529 47.5349 47.9929 48.3289 46.9009 47.3079 47.7779 48.2179 48.6519 49.0149 27.8019 27.7299 27.7059 27.5919 27.5189 27.5429 23.3509 23.4699 23.5709 23.4709 23.4329 23.3769

20.7449 20.7449 20.8539 20.9539 21.2509 21.3629 20.0289 19.9649 19.8839 19.8289 19.7719 19.5889 10.6489 10.4199 10.1539 09.9549 0.97379 09.5319 10.4179 10.1279 09.8689 09.7429 09.6049 09.4729

4.0 4.0 5.0 5.0 6.0 6.0 3.0 6.0 5.0 5.0 7.0 8.0 5.0 6.0 7.0 8.0 9.0 9.0 3.0 3.0 4.0 4.0 5.0 8.0

Temperature uC

30.0 30.0 30.0 29.9 30.0 29.9 30.1 30.1 29.9 30.0 30.0 30.0 30.0 30.0 30.0 30.1 30.1 30.1 29.7 29.8 29.9 29.9 29.9 30.0

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

0.7 0.7 0.6 0.7 0.7 0.7 0.7 0.7 0.7 0.7 0.7 0.6 0.8 0.9 0.8 0.7 0.7 0.6 0.8 0.8 0.7 0.6 0.6 0.6

Dissolved Salinity % oxygen mg/L

29.5 29.7 29.7 29.9 30.0 30.1 29.6 29.6 29.6 29.6 29.6 29.6 29.6 29.6 29.6 29.5 29.6 29.6 27.7 29.4 29.4 29.4 29.4 29.5

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

(95%) clearly dominated the assemblages at stations in Group A1, followed by Elphidium at 3%, resulting in a significantly (ANOVA, p , 0.05) low mean FoRAM Index (1.01) and high AEI (98). Group A1 sediments were characterized by a relatively high mean percentage of organic matter (17%) and relatively low silt and clay (42%). The seven samples making up Group A2 were mainly collected in Pantai Acheh. The mean density of foraminifera (Fig. 5) found here was 57 individuals/cm3, and diversity was relatively low (H9 5 0.37). Group A2 assemblages were characterized by high dominance of Ammonia (93%), followed by Elphidium (2%) and Bolivina (1%), producing a FoRAM index of 1.09 and AEI of 97. The sediments at Group A2 stations were very muddy (99%); the mean organic-matter concentration in the sediments was 11%. Group B1 included the largest number of samples (66), which were collected from 11 stations scattered among all four sites. These stations (Fig. 5) were characterized by intermediate density (mean: 42 individuals/cm3) and diver-

0.7 0.5 0.5 0.8 1.2 1.6 0.5 0.5 0.6 0.6 0.5 0.6 0.5 0.5 0.6 0.7 0.5 0.5 2.7 0.6 0.6 0.6 0.6 0.6

5.5 5.2 5.4 5.1 5.2 5.1 5.1 5.3 5.2 4.8 4.7 5.2 4.9 5.2 5.3 5.5 5.4 5.5 5.0 5.3 5.3 5.3 5.4 5.3

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

0.6 0.9 1.0 1.0 0.8 0.8 0.9 0.9 0.9 1.1 1.1 1.0 1.7 1.1 1.0 1.0 0.8 0.7 1.4 1.1 1.2 1.0 0.8 0.9

Organic matter %

pH

8.3 8.4 8.5 8.4 8.5 8.5 8.4 8.5 8.5 8.4 8.5 8.5 8.5 8.5 8.5 8.5 8.5 8.5 8.4 8.3 8.4 8.4 8.5 8.4

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

0.2 0.2 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.2 0.2 0.1 0.1 0.1 0.1

Sand %

19.5 6 12.5 77.4 6 2.4 12.2 6 5.2 22.3 6 1.0 10.6 6 2.6 2.2 6 1.0 6.2 6 1.6 1.1 6 0.1 8.8 6 2.8 1.0 6 0.2 9.6 6 3.8 1.1 6 0.4 14.8 6 6.3 39.1 6 4.0 11.0 6 3.6 2.2 6 0.7 7.8 6 1.7 0.9 6 0.1 6.9 6 2.6 1.9 6 0.1 7.8 6 1.4 1.1 6 0.1 8.1 6 0.8 0.7 6 0.3 14.7 6 7.6 2.7 6 1.4 13.8 6 6.4 2.4 6 0.3 14.7 6 10.0 1.8 6 0.1 7.7 6 2.4 1.7 6 0.2 10.2 6 3.7 1.3 6 0.1 9.4 6 3.2 0.6 6 0.0 16.7 6 7.2 1.3 6 0.4 12.8 6 3.8 0.6 6 0.1 10.3 6 3.0 0.7 6 0.2 7.5 6 1.5 0.9 6 0.0 10.5 6 1.2 0.6 6 0.0 10.3 6 1.8 0.6 6 0.1

Silt %

22.6 77.7 97.8 98.9 99.0 98.9 60.9 97.8 99.1 98.1 98.9 99.3 97.3 97.6 98.2 98.3 98.7 99.4 98.7 99.4 99.3 99.1 99.4 99.4

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

2.4 1.0 1.0 0.1 0.2 0.0 4.0 0.7 0.1 0.1 0.1 0.3 1.4 0.3 0.1 0.2 0.1 0.0 0.4 0.1 0.2 0.0 0.0 0.1

sity (mean: H950.45). Ammonia dominated the assemblages, but with a slightly lower percentage (90%), followed by Ammobaculites (4%), resulting in a mean FoRAM Index of 1.09 and AEI of 97. Group B1 sediments had the least organic matter (9.7%) of all groups, while the mean percentage of silt and clay was high (97%). Group B2 consists of samples collected only from Teluk Ketapang. This group had the lowest mean density of benthic foraminifera (7 individuals/cm3) and the highest diversity of the four sampling sites (H950.56). It had a significantly higher mean FoRAM index (1.23) and lower AEI index (79). The sediments were very muddy, with more than 98% silt and clay and 11% organic matter. DISCUSSION The environmental parameters revealed that the study area is hyposaline with muddy sediments (with one exception) and substantial proportions of organic matter.

TABLE 2. Malaysia Marine Water Quality Criteria and Standards (excerpted from Malaysian Meteorological Department, 2010). Parameter

Beneficial uses

Class 1

Preservation, Marine Protected Areas, Marine Parks Dissolved oxygen (mg/L) .80% saturation Ammonia (mg/L) 0.035 Nitrite (mg/L) 0.010 Nitrate (mg/L) 0.010 Phosphate (mg/L) 0.005 Total suspended solids 25 mg/L or #10% increase (mg/L) in seasonal average, whichever is lower

Class 2

Class 3

Marine Life, Fisheries, Ports, Oil & Gas Fields Coral Reefs, Recreational and Mariculture 5 3 0.070 0.320 0.055 1.000 0.060 1.000 0.075 0.670 50 mg/L (25 mg/L) or #10% 100 mg/L or #10% increase increase in seasonal in seasonal average, average, whichever is lower whichever is lower

Class E

Mangrove Estuarine & River-mouth Water 4 0.070 0.055 0.060 0.075 100 mg/L or #30% increase in seasonal average, whichever is lower

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FIGURE 3. The distribution of organic matter (high ,34%, low ,3%) along the transects in Teluk Bahang (TB), Teluk Aling (TA), Teluk Ketapang (TK), and Pantai Acheh (PA) during the sampling period October 2010–September 2011. Transect station names are shown in Figure 2.

The measured physical and chemical parameters showed no significant differences among sampling sites or stations (ANOVA, p ,0.05). The consistency of these parameters favors euryhaline taxa, which are often stress tolerant. Domination by certain foraminiferal taxa is a common response to environmental stress, including pollution (Armynot du Chaˆtelet et al., 2004).The overwhelming predominance of Ammonia in the sample set is consistent with hyposaline subtropical/tropical coastal lagoons similar to those studied by Seiglie (1971), Poag (1981), Ishman et al. (1997), Tsujimoto et al. (2006), and many others. The generally low diversities (e.g., Buosi et al., 2010) and FoRAM indices (e.g., Carnahan et al., 2009), and high AEI (e.g., Sen Gupta et al., 1996) reflect the tropical hyposaline coastal-lagoon conditions. What appears to best reflect anthropogenic input is test density, which is consistent with the Alve (1995) model of decreasing densities with distance from a pollution source. Densities are highest and diversities lowest nearshore in the stations of Teluk Bahang and Teluk Aling, which are most influenced by human activities (Group A1). Densities are nearly an order of magnitude lower at the more offshore Group B1 sites, except for stations in Teluk Bahang which still shows a density peak at 600 m from shore, and the less

impacted sites in Teluk Ketapang (Group B2). Meanwhile densities and diversities are intermediate at Pantai Acheh, represented by Group A2. While percent organic matter is high in the sediment samples, with means at all stations .6%, the source and composition of the organic matter may be critical to foraminiferal abundance. Organic matter from mangroves is relatively refractory compared to organic matter from marine sources (e.g., Newell et al., 1995; Luz et al., 2010). Moreover, Yanko et al. (2003) noted that the organic matter from sewage and aquaculture is readily metabolized by marine organisms and therefore can promote foraminiferal blooms. The foraminiferal tests found in Group A1 also tended to be larger, which can indicate an organically polluted area (Yanko et al., 1994). In addition, the shallow depth and sandier sediment at Group A1 sites indicates more hydrodynamic influence, which also may have winnowed out smaller tests. Group B2 samples, from Teluk Ketapang had the lowest foraminiferal abundances and the highest diversities. Consistent with those parameters, this group is characterized by the lowest abundance (both relative and absolute) of Ammonia. Overall, the H9, FoRAM, and AEI indices point to stress at all sites, the least impacted being Teluk Ketapang.

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FIGURE 4. Dendrogram from hierarchical cluster analysis and the association of cluster groups with FoRAM Index, Ammonia-Elphidium Index (AEI), Shannon diversity index (H9), and % organic matter.

CONCLUSIONS The regional salinity and sedimentary conditions appear to be the major influences on benthic environments in coastal waters of Penang National Park and the surrounding area. Although naturally occurring hyposalinity, muddy sediments, and relative high organic-matter loading are evident throughout the study area, the foraminiferal assemblages revealed that the sediment quality is affected by proximity to anthropogenic activities. The high level of organic matter promotes abundance and domination of stress-tolerant foraminifera, especially Ammonia whose abundance was highest closer to shore and declined seaward. This study again demonstrates the utility of foraminiferal assemblages as bioindicators in monitoring

of coastal waters, as they can be used to distinguish between natural and anthropogenically induced conditions. Our results suggest a testable hypothesis that, while organic matter is relatively prevalent everywhere, anthropogenic inputs provide more readily metabolized organic matter that can promote elevated abundances of the most stresstolerant taxa, especially Ammonia. ACKNOWLEDGMENTS We thank the Universiti Sains Malaysia for funding this research under the Research University Grant 1001/ PPANTAI/815052 and the Centre for Marine and Coastal Studies for the great facilities. We also acknowledge all

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FIGURE 5.

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Mean density (individuals/cm3) of foraminifera according to cluster groups.

field and laboratory assistants for their help during sample collection. We are grateful to Pamela Hallock, N. Rajeshwara Rao, and an anonymous reviewer for their helpful and critical reviews of the manuscript and editor Paul Brenckle. REFERENCES Alve, E., 1995, Benthic foraminiferal responses to estuarine pollution: a review: Journal of Foraminiferal Research, v. 25, p. 190–203. Armynot du Chaˆtelet, E., Debenay, J.-P., and Soulard, R., 2004, Foraminiferal proxies for pollution monitoring in moderately polluted harbors: Environmental Pollution, v. 127, p. 27–40. Bale, A. J., and Kenny, A. J., 2005, Sediment analysis and seabed characterisation, in Eleftheriou, A., and Mcintyre, A. (eds.), Methods for the Study of Marine Benthos, 3rd Edition: Blackwell Science Ltd., Oxford, p. 43–81. Barbosa, C. F., Prazeres, M. F., Ferreira, B. P., and Seoane, J. C. S., 2009, Foraminiferal assemblage and reef check census in coral reef health monitoring of east Brazilian margin: Marine Micropaleontology, v. 73, p. 62–69. Buosi, C., Frontalini, F., Da Pelo, S., Cherchi, A., Coccioni, R., and Bucci, C., 2010, Foraminifera proxies for environmental monitoring in the polluted lagoon of Santa Gilla Cagliari, Italy: Present Environment and Sustainable Development, v. 4, p. 91–103. Carnahan, E. A., Hoare, A. M., Hallock, P., Lidz, B. H., and Reich, C. D., 2009, Foraminiferal assemblages in Biscayne Bay, Florida, USA: responses to urban and agricultural influence in a subtropical estuary: Marine Pollution Bulletin, v. 59, p. 221–233. Chua, T., Gorre, I. R. L., Bernad, S. R., Gervacio, B., and Ebariva, M. C., 2000, The Malacca Straits: Marine Pollution Bulletin, v. 416, p. 160–178. Cushman, J. A., 1928, Foraminifera: their classification and economic use: Cushman Laboratory for Foraminiferal Research, Special Publication No. 1, p. 1–53. Hallock, P., Lidz, B. H., Cockey-Burkhard, E. M., and Donnelly, K. B., 2003, Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM Index: Environmental Monitoring and Assessment, v. 81, p. 221–238. Hulings, N. C., and Gray, J. S., 1971, A manual for the study of the meiofauna: Smithsonian Contribution to Zoology, No. 27, p. 78–84. Ishman, S. E., Graham, S., and D’Ambrosio, J., 1997, Modern benthic foraminifera distributions in Biscayne Bay: analogs for historical

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Tsujimoto, A., Nomura, R., Yasuhara, M., Yamazaki, H., and Yoshikawa, S., 2006, Impact of eutrophication on shallow marine benthic foraminifers over the last 150 years in Osaka Bay, Japan: Marine Micropaleontology, v. 60, p. 258–268. Yanko, V., Kronfeld, J., and Flexer, A., 1994, Response of benthic foraminifera to various pollution sources: implications for pollution monitoring: Journal of Foraminiferal Research, v. 24, p. 1–17. Yanko, V., Arnold, A. J., and Parker, W. C., 2003, Effect of marine pollution on benthic foraminifera, in Sen Gupta, B. K. (ed.), Modern Foraminifera: Kluwer Academic Publishers, Dordrecht, p. 217–234. Received 25 March 2013 Accepted 28 November 2013