BENTHIC FORAMINIFERAL DISTRIBUTIONS AS BIOINDICATORS INCOASTAL WATERS OF PENANG NATIONAL PARK, MALAYSIA

FATIN I. MINHAT1,4, KHAIRUN YAHYA

2, ANITA TALIB3

AND OMAR AHMAD1

ABSTRACT

The distribution and abundance of benthic foraminiferawere studied along the coastal waters of Penang NationalPark, Malaysia, at four sites (Teluk Bahang, Teluk Aling,Teluk Ketapang, and Pantai Acheh) representative of varyinglevels of anthropogenic activities. A total of 144 sediment andwater samples was collected and environmental parametersmeasured bimonthly between October 2010–September 2011along four transects at 200-m intervals from the low-tide lineto 1200 m offshore. Sediments were mostly muddy andcontained substantial organic matter (typically .7%); waterswere warm (,30uC) and somewhat brackish (,29–30%).Specimens of the stress-tolerant genera Ammonia andElphidium dominated assemblages along all transects. Clusteranalysis separated the stations into four groups. The GroupA1 stations (200 m offshore of Teluk Bahang and TelukAling) were characterized by the sandiest sediments, highestorganic sediment concentrations (17%), a tendency forhypoxia [mean Ammonia-Elphidium Index (AEI) = 98],highest foraminiferal abundances (mean: 359 individuals/cm3), and relatively low diversities (mean H9= 0.25). GroupA2 included mostly Pantai Acheh stations, where meanconcentration of organic matter (11%) and foraminiferaldensity (57 individuals/cm3) were lower than in Group A1stations, diversity was slightly higher (H9= 0.37), and the AEIwas similar (97). Group B1 represented the most stationsfrom 11 sites in Teluk Bahang, Teluk Aling, and TelukKetapang, and had the lowest mean organics (9.7%) andintermediate densities (42 individuals/cm3) and diversities(H9= 0.45). Group B2 included only the Teluk Ketapangstations furthest from shore, with the lowest mean foraminif-eral densities (7 individuals/cm3) and AEI (79) and the highestdiversities (H9= 0.56). The Teluk Ketapang site was also theleast subject to anthropogenic stressors. The spatial distribu-tions of foraminifera appeared to reflect the sedimentaryenvironment and input of labile organic matter fromanthropogenic sources.

INTRODUCTION

Benthic organisms, both macrofauna and meiofauna,have long been recognized as good bioindicators due totheir limited movement, which can expose them topollutants for prolonged periods. Benthic foraminifera arehighly abundant meiofauna, sometimes making up 80% ofthe biomass (Snider et al., 1984), and are ubiquitous innearly all marine environments (Sen Gupta, 2003). Their

distribution is mainly affected by environmental factors intheir microhabitat. The interplay among physical, chemical,and biological conditions allows certain species to thrive,while excluding others (Jorissen, 2003). Benthic fora-minifera are used in many efforts to monitor biological,chemical, and thermal pollution (Alve, 1995). Theirabundance, preservation potential, diversity, environmentaltolerances, wide distribution, and cost effective samplecollecting have made foraminifera excellent monitoringindicators (Alve, 1995; Scott et al., 2001; Murray, 2006).This study uses physical and chemical parameters togetherwith foraminiferal assemblages and distributions to assesscoastal waters and sediment quality around PenangNational Park.

STUDY AREA

The study was conducted in the coastal waters of PenangNational Park, Penang Island, Malaysia (Fig. 1) at foursampling sites: Teluk Bahang, Teluk Aling, Teluk Keta-pang, and Pantai Acheh. The depth ranged between 1.5–10 m, with predominantly muddy substrate at moststations. These coastal waters are influenced by twoprevailing seasons from the northeast and southwest (Chuaet. al., 2000). The northeast one brings monsoon rain fromDecember–February, while during the southwest season(June–August) the island experiences dry weather.

Sampling sites were based on the nature of humanactivities present within the region. Inshore fishing andfloating-cage aquaculture are major economic activities inTeluk Bahang. Teluk Aling is situated in a sheltered coastalarea next to Teluk Bahang. The only human activitiesnearby are related to the Centre for Marine and CoastalStudies (CEMACS), Universiti Sains Malaysia. TelukKetapang is a sheltered bay situated 3 km southwest ofTeluk Bahang. There is no development along its intertidalarea, and therefore, it is considered a less disturbed site.Finally the Pantai Acheh sampling site is situated furthersouth, closer to the mangrove ecosystem (Balik Pulau) ofthe Pinang River. Major anthropogenic activities occurnear Pantai Acheh, as mangroves has been cleared foraquaculture ponds and housing, and thereby contribute tothe effluent (domestic, aquaculture, and agriculture) dis-charge into the river (Nurul Ruhayu, 2011).

MATERIALS AND METHODS

One hundred forty-four sediment and water samples werecollected bimonthly between October 2010 and September2011. These samples together with in situ measurements oftemperature, salinity, dissolved oxygen, and pH wereobtained along a transect (Fig. 2) from the low-tide lineto 1200 m offshore at 200-m intervals. Bulk sediments werecollected 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, 11800Penang, Malaysia

4 Correspondence author. E-mail: fim98181@hotmail.my

Journal of Foraminiferal Research, v. 44, no. 2, p. 143–150, April 2014

143

immediately subsampled using a hand corer with 5-cminner diameter and transferred to 250-ml pre-labelledcontainers. Samples were then fixed with 4% bufferedformalin to minimize foraminiferal test degradation (Hul-ings & Gray, 1971). Water samples from ,1 m above theseafloor were collected with a water sampler (HorizontalTransparent Acrylic 2.2 L), stored in 1-L polyethylenebottles, and taken to the laboratory for further analysis.From each preserved sediment sample, two 8-cm3 subsam-ples were taken randomly for quantitative analysis offoraminifera. The subsamples were wet-sieved using 1000-mm and 63-mm sieves. The residue on the 63-mm sieve wascarefully transferred into a 10-cm3 counting chamber usingdistilled water, and picked with a fine artist’s brush

(Somerfield et al., 2005). Counting and sorting werecompleted with the aid of a dissecting microscope (MeijiEMZ 57378). Total foraminiferal densities were based onsediment volume (cm3). Generic identification was basedon Millet (1899), Cushman (1928), Loeblich & Tappan(1987), and Sen Gupta (2003). Selected samples were driedand photographed with a Carl Zeiss SMT scanningelectron microscope.

Several indices were calculated using the foraminiferalassemblage 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 Ammonia-Elphidium Index (AEI) of Sen Gupta et al. (1996).

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).

144 MINHAT AND OTHERS

Sea-water samples were analyzed for nutrient content(nitrate, ammonium, nitrite, and phosphate) and totalsuspended solids, based on the methods of Strickland &Parsons (1972). Grain-size analysis followed the procedureof Bale & Kenny (2005). The loss on ignition (LOI) methodwas used to determine the percentages of organic matter insediment (Bale & Kenny, 2005). Cluster analysis wascarried out to interpret the response of foraminiferalassemblages to the environmental gradients (Murray,2006).

RESULTS

Fourteen foraminiferal genera were identified in thisstudy. 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%), Egger-ella (1.5%), Hopkinsina (1%), and Asterorotalia (1%). Mostgenera were found at all sampling sites except forHopkinsina that was not detected from Teluk Bahang andTeluk Ketapang, and Quinqueloculina, Lagena, and Aster-orotalia that were absent at Teluk Bahang.

The mean values for environmental parameters are givenin 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%) throughoutthis study indicated coastal salinities typical of westpeninsular Malaysia. Nutrient analysis showed the meanconcentration 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. Theseconcentrations indicate that water quality at all sites couldpotentially fall into Class 2, according to the MalaysiaMarine Water Quality Criteria and Standard (excerptedfrom the Malaysian Meteorological Department, 2010;Table 2).

Organic matter was abundant in most sediment samples,ranging from ,3–34%. Concentrations of organic matterwere generally higher closer to the shore (mean 16.4% 6 1.7at 200 m; p , 0.05, Tukey’s test), decreasing significantly(mean 7.07% 6 0.41) at 800 m from shore toward the opensea. Figure 3 shows the distribution of organic matter alongall transects throughout the sampling months.

CLUSTER ANALYSIS

The Q-mode hierarchical cluster analysis produced twomajor groups (A and B) with subgroups (A1, A2, B1, andB2; Fig. 4). Group A1 is comprised of samples from twostations located 200 m from shore in Teluk Bahang andTeluk Aling. This group has extremely high mean density(359 individuals/cm3) but low diversity (H95 0.25). Ammonia

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

BENTHIC FORAMINIFERA AS BIOINDICATORS 145

(95%) clearly dominated the assemblages at stations inGroup A1, followed by Elphidium at 3%, resulting in asignificantly (ANOVA, p , 0.05) low mean FoRAM Index(1.01) and high AEI (98). Group A1 sediments werecharacterized by a relatively high mean percentage of organicmatter (17%) and relatively low silt and clay (42%).

The seven samples making up Group A2 were mainlycollected in Pantai Acheh. The mean density of foraminif-era (Fig. 5) found here was 57 individuals/cm3, anddiversity was relatively low (H9 5 0.37). Group A2assemblages were characterized by high dominance ofAmmonia (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 thesediments was 11%.

Group B1 included the largest number of samples (66),which were collected from 11 stations scattered among allfour sites. These stations (Fig. 5) were characterized byintermediate density (mean: 42 individuals/cm3) and diver-

sity (mean: H950.45). Ammonia dominated the assemblag-es, but with a slightly lower percentage (90%), followed byAmmobaculites (4%), resulting in a mean FoRAM Index of1.09 and AEI of 97. Group B1 sediments had the leastorganic matter (9.7%) of all groups, while the meanpercentage of silt and clay was high (97%).

Group B2 consists of samples collected only fromTeluk Ketapang. This group had the lowest mean den-sity of benthic foraminifera (7 individuals/cm3) and thehighest 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 verymuddy, with more than 98% silt and clay and 11% organicmatter.

DISCUSSION

The environmental parameters revealed that the studyarea is hyposaline with muddy sediments (with oneexception) and substantial proportions of organic matter.

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 mTemperature

uC Salinity %Dissolved

oxygen mg/L pHOrganic

matter % Sand % Silt %

TB200 46.3789 20.7449 4.0 30.0 6 0.7 29.5 6 0.7 5.5 6 0.6 8.3 6 0.2 19.5 6 12.5 77.4 6 2.4 22.6 6 2.4TB400 46.7579 20.7449 4.0 30.0 6 0.7 29.7 6 0.5 5.2 6 0.9 8.4 6 0.2 12.2 6 5.2 22.3 6 1.0 77.7 6 1.0TB600 47.1529 20.8539 5.0 30.0 6 0.6 29.7 6 0.5 5.4 6 1.0 8.5 6 0.1 10.6 6 2.6 2.2 6 1.0 97.8 6 1.0TB800 47.5349 20.9539 5.0 29.9 6 0.7 29.9 6 0.8 5.1 6 1.0 8.4 6 0.2 6.2 6 1.6 1.1 6 0.1 98.9 6 0.1TB1000 47.9929 21.2509 6.0 30.0 6 0.7 30.0 6 1.2 5.2 6 0.8 8.5 6 0.1 8.8 6 2.8 1.0 6 0.2 99.0 6 0.2TB1200 48.3289 21.3629 6.0 29.9 6 0.7 30.1 6 1.6 5.1 6 0.8 8.5 6 0.1 9.6 6 3.8 1.1 6 0.4 98.9 6 0.0TA200 46.9009 20.0289 3.0 30.1 6 0.7 29.6 6 0.5 5.1 6 0.9 8.4 6 0.1 14.8 6 6.3 39.1 6 4.0 60.9 6 4.0TA400 47.3079 19.9649 6.0 30.1 6 0.7 29.6 6 0.5 5.3 6 0.9 8.5 6 0.1 11.0 6 3.6 2.2 6 0.7 97.8 6 0.7TA600 47.7779 19.8839 5.0 29.9 6 0.7 29.6 6 0.6 5.2 6 0.9 8.5 6 0.1 7.8 6 1.7 0.9 6 0.1 99.1 6 0.1TA800 48.2179 19.8289 5.0 30.0 6 0.7 29.6 6 0.6 4.8 6 1.1 8.4 6 0.2 6.9 6 2.6 1.9 6 0.1 98.1 6 0.1TA1000 48.6519 19.7719 7.0 30.0 6 0.7 29.6 6 0.5 4.7 6 1.1 8.5 6 0.1 7.8 6 1.4 1.1 6 0.1 98.9 6 0.1TA1200 49.0149 19.5889 8.0 30.0 6 0.6 29.6 6 0.6 5.2 6 1.0 8.5 6 0.1 8.1 6 0.8 0.7 6 0.3 99.3 6 0.3TK200 27.8019 10.6489 5.0 30.0 6 0.8 29.6 6 0.5 4.9 6 1.7 8.5 6 0.1 14.7 6 7.6 2.7 6 1.4 97.3 6 1.4TK400 27.7299 10.4199 6.0 30.0 6 0.9 29.6 6 0.5 5.2 6 1.1 8.5 6 0.1 13.8 6 6.4 2.4 6 0.3 97.6 6 0.3TK600 27.7059 10.1539 7.0 30.0 6 0.8 29.6 6 0.6 5.3 6 1.0 8.5 6 0.1 14.7 6 10.0 1.8 6 0.1 98.2 6 0.1TK800 27.5919 09.9549 8.0 30.1 6 0.7 29.5 6 0.7 5.5 6 1.0 8.5 6 0.1 7.7 6 2.4 1.7 6 0.2 98.3 6 0.2TK1000 27.5189 0.97379 9.0 30.1 6 0.7 29.6 6 0.5 5.4 6 0.8 8.5 6 0.1 10.2 6 3.7 1.3 6 0.1 98.7 6 0.1TK1200 27.5429 09.5319 9.0 30.1 6 0.6 29.6 6 0.5 5.5 6 0.7 8.5 6 0.2 9.4 6 3.2 0.6 6 0.0 99.4 6 0.0PA200 23.3509 10.4179 3.0 29.7 6 0.8 27.7 6 2.7 5.0 6 1.4 8.4 6 0.2 16.7 6 7.2 1.3 6 0.4 98.7 6 0.4PA400 23.4699 10.1279 3.0 29.8 6 0.8 29.4 6 0.6 5.3 6 1.1 8.3 6 0.2 12.8 6 3.8 0.6 6 0.1 99.4 6 0.1PA600 23.5709 09.8689 4.0 29.9 6 0.7 29.4 6 0.6 5.3 6 1.2 8.4 6 0.1 10.3 6 3.0 0.7 6 0.2 99.3 6 0.2PA800 23.4709 09.7429 4.0 29.9 6 0.6 29.4 6 0.6 5.3 6 1.0 8.4 6 0.1 7.5 6 1.5 0.9 6 0.0 99.1 6 0.0PA1000 23.4329 09.6049 5.0 29.9 6 0.6 29.4 6 0.6 5.4 6 0.8 8.5 6 0.1 10.5 6 1.2 0.6 6 0.0 99.4 6 0.0PA1200 23.3769 09.4729 8.0 30.0 6 0.6 29.5 6 0.6 5.3 6 0.9 8.4 6 0.1 10.3 6 1.8 0.6 6 0.1 99.4 6 0.1

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

Parameter Class 1 Class 2 Class 3 Class E

Beneficial uses Preservation, MarineProtected Areas,Marine Parks

Marine Life, Fisheries,Coral Reefs, Recreationaland Mariculture

Ports, Oil & Gas Fields Mangrove Estuarine &River-mouth Water

Dissolved oxygen (mg/L) .80% saturation 5 3 4Ammonia (mg/L) 0.035 0.070 0.320 0.070Nitrite (mg/L) 0.010 0.055 1.000 0.055Nitrate (mg/L) 0.010 0.060 1.000 0.060Phosphate (mg/L) 0.005 0.075 0.670 0.075Total suspended solids

(mg/L)25 mg/L or #10% increase

in seasonal average,whichever is lower

50 mg/L (25 mg/L) or #10%increase in seasonalaverage, whichever is lower

100 mg/L or #10% increasein seasonal average,whichever is lower

100 mg/L or #30% increasein seasonal average,whichever is lower

146 MINHAT AND OTHERS

The measured physical and chemical parameters showed nosignificant differences among sampling sites or stations(ANOVA, p ,0.05). The consistency of these parametersfavors euryhaline taxa, which are often stress tolerant.

Domination by certain foraminiferal taxa is a commonresponse to environmental stress, including pollution(Armynot du Chatelet et al., 2004).The overwhelmingpredominance of Ammonia in the sample set is consistentwith hyposaline subtropical/tropical coastal lagoons similarto those studied by Seiglie (1971), Poag (1981), Ishmanet al. (1997), Tsujimoto et al. (2006), and many others. Thegenerally low diversities (e.g., Buosi et al., 2010) andFoRAM indices (e.g., Carnahan et al., 2009), and high AEI(e.g., Sen Gupta et al., 1996) reflect the tropical hyposalinecoastal-lagoon conditions.

What appears to best reflect anthropogenic input is testdensity, which is consistent with the Alve (1995) model ofdecreasing densities with distance from a pollution source.Densities are highest and diversities lowest nearshore in thestations of Teluk Bahang and Teluk Aling, which are mostinfluenced by human activities (Group A1). Densities arenearly an order of magnitude lower at the more offshoreGroup B1 sites, except for stations in Teluk Bahang whichstill shows a density peak at 600 m from shore, and the less

impacted sites in Teluk Ketapang (Group B2). Meanwhiledensities and diversities are intermediate at Pantai Acheh,represented by Group A2.

While percent organic matter is high in the sedimentsamples, with means at all stations .6%, the source andcomposition of the organic matter may be critical toforaminiferal abundance. Organic matter from mangrovesis relatively refractory compared to organic matter frommarine sources (e.g., Newell et al., 1995; Luz et al., 2010).Moreover, Yanko et al. (2003) noted that the organicmatter from sewage and aquaculture is readily metabolizedby marine organisms and therefore can promote forami-niferal blooms. The foraminiferal tests found in Group A1also tended to be larger, which can indicate an organicallypolluted area (Yanko et al., 1994). In addition, the shallowdepth and sandier sediment at Group A1 sites indicatesmore hydrodynamic influence, which also may havewinnowed out smaller tests.

Group B2 samples, from Teluk Ketapang had the lowestforaminiferal abundances and the highest diversities. Con-sistent with those parameters, this group is characterized bythe lowest abundance (both relative and absolute) ofAmmonia. Overall, the H9, FoRAM, and AEI indices pointto stress at all sites, the least impacted being Teluk Ketapang.

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

BENTHIC FORAMINIFERA AS BIOINDICATORS 147

CONCLUSIONS

The regional salinity and sedimentary conditions appearto be the major influences on benthic environments incoastal waters of Penang National Park and the surround-ing area. Although naturally occurring hyposalinity, muddysediments, and relative high organic-matter loading areevident throughout the study area, the foraminiferalassemblages revealed that the sediment quality is affectedby proximity to anthropogenic activities. The high level oforganic matter promotes abundance and domination ofstress-tolerant foraminifera, especially Ammonia whoseabundance was highest closer to shore and declinedseaward. This study again demonstrates the utility offoraminiferal assemblages as bioindicators in monitoring

of coastal waters, as they can be used to distinguish betweennatural and anthropogenically induced conditions. Ourresults suggest a testable hypothesis that, while organicmatter is relatively prevalent everywhere, anthropogenicinputs provide more readily metabolized organic matterthat can promote elevated abundances of the most stress-tolerant taxa, especially Ammonia.

ACKNOWLEDGMENTS

We thank the Universiti Sains Malaysia for funding thisresearch under the Research University Grant 1001/PPANTAI/815052 and the Centre for Marine and CoastalStudies for the great facilities. We also acknowledge all

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.

148 MINHAT AND OTHERS

field and laboratory assistants for their help duringsample collection. We are grateful to Pamela Hallock, N.Rajeshwara Rao, and an anonymous reviewer for theirhelpful and critical reviews of the manuscript and editorPaul Brenckle.

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Received 25 March 2013Accepted 28 November 2013

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