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African Journal of Biotechnology Vol. 9(39), pp. xxx-xxx, 27 September, 2010 Available online at http://www.academicjournals.org/AJB ISSN 1684­5315 ©2010 Academic Journals

Full Length Research Paper

Studies on the benthic macroinvertebrates diversity species as bio-indicators of environmental health in Bahrekan Bay (Northwest of Persian Gulf)

Maryam Mohammadi Roozbahani1*, Seyed Mohammad Bagher Nabavi2, Parvin Farshchi1 and Abdolrahman Rasekh3

1

Department of Environmental Science, Graduate School of the Environment, Science and Research Branch, Islamic Azad University, Tehran, Iran. 2 Department of Marine Biology, University of Marine Science and Technology, Khoramshahr, Iran. 3 Department of Statistics, Shahid Chamran University, Ahwaz, Iran.

Accepted 23 August, 2010

The purpose of this study is to evaluate the seasonal diversity of benthic macroinvertebrates in the Bahrekan bay (situated in the northwest of the Persian Gulf) using diversity and evenness indices. Physiochemical parameters of water, grain size analysis and percentage total organic matter (TOM) of sediment were assessed during four seasons. Hence, the samples of benthic macroinvertebrate and sediment were obtained from fifteen sites along the Bahrekan Bay, from November 2008 to August 2009. The diversity of benthic macroinvertebrates in fifteen sites was calculated. Also, the differences between physico-chemical parameters of sea water, percentage TOM and grain size of sediment and diversity indices were determined (P = 0.05). The diversity of all stations was compared with each other in each season. The correlation coefficients of all above parameters were determined. The highest diversity was obtained in winter (Simpsson index: 0.13 ± 0.01, H´: 3.47 ± 0.06) and the lowest diversity was obtained in autumn (Simpson index: 0.16 ± 0.01, H´:3.17 ± 0.06). The annual mean of Simpson diversity index was 0.15 ± 0.04 which indicated that macrobenthose in Bahrekan bay have a good variation. The results of Shanon­Wiener, Brilluin and N1 (number of equally common species) indices confirmed the results of Simpson index. In stations where diversity had little fluctuations based on N1 index, the degree of the fluctuations were more recognizable. At stations near the shoreline, the diversity indices was categorized as moderate pollution (H´: 1 - 3) due to the fishing activities. Key words: Benthic macroinvertebrate, biological indicators, species diversity, ecological status, Persian Gulf. INTRODUCTION Marine and estuarine due to their ecological and economical roles in the ecosystem, are one of the most important environmental habitats. Macrobenthose communities contain important part of aquatic organisms in marine environments. The aquatic organisms are exposed to anthropogenic disturbances as well as natural changes in their habitats which cause them to react in different ways. Therefore, aquatic organisms have an important role in bioassessment (Mooraki et al., 2009; Girgin, 2010). In addition, subtidal habitats are known as important marine ecosystems because they can be considered as breeding and nursery areas for many marine organisms (Mooraki et al., 2009). Macrobenthose diversity is closely related to both environmental factors and anthropogenic alterations (Nouri et al., 2008). Diversity indices are generally scalar ecological indicators. Using these indices is common in ecological analysis. Species diversity indicates the status of the ecosystems (Izsak, 2007). Macrobenthic assemblages have been used to indicate stress as they are sensitive to pollution and are also different due to the sensitivity degree. Based on sensitivity

*Corresponding author. E-mail: [email protected] yahoo.com.

Table 1. Seasonal mean of physico-chemical parameters of sea water.

Season Autumn Winter Spring Summer Total

T(° C) Mean ±SEM a 18.66±0.07 16.04±0.03b 25.64±0.02c 30.38±0.01d 22.67±0.74

DO(mg/L) Mean ±SEM a 5.94±0.03 8.15±0.03b 5.63±0.01c 4.84±0.01d 6.14±0.16

Salinity (PSU) Mean ±SEM a 53.51±0.21 49.84±0.11b 45.31±0.08c 40.46±0.11d 47.28±0.64

pH (units) Mean ±SEM a 8.5±0.005 8.44±0.01b 8.42±0.00b 8.34±0.00d 8.42±0.08

EC(µs) Mean ±SEM a 66.55±0.13 68.13±0.07b 68.69±0.03c 70.02±0.06d 68.35±0.17

Different superscripts within the same column are significantly different at P < 0.05.

degree, 5 ecological groups can be considered (Gesteira and Dauvin, 2000; Muxika et al., 2005). These species detect the effects of different pollutants and disturbances over the relatively long periods of months to years and they are reliable because their life-cycle is attributed to recruitment potential and long life of organisms. The reason for their responses to pollution is that benthic organisms live in sediment and are able to accumulate contaminants over long periods; also these organisms can not move and migrate due to environmental pressures and disturbances (Paul et al., 2001). Macrobenthose species have been used for decades to measure and describe ecological status and variations of marine and estuarine environments (Angradi et al., 2001; Manoliadis, 2002; Alam et al., 2007; Sivadas et al, 2008). The extent and intensity of human disturbances to oceanic ecosystems is a significant threat to both structural and functional biodiversity and in many cases, this has virtually eliminated the natural systems which may serve as baselines to evaluate these impacts (Simon and Paul, 2002). Various studies based on benthic macroinvertebrates have been conducted in the Persian Gulf (Nabavi, 1992; Parsamanesh, 1994). Bahrekan Bay is one of the most important sites for fishing activities. Mud flats of Bahrekan Bay are suitable habitats for many fish species because it has a high capacity of biota potential. Also, it is one of the most important oil fields in Iran located in Bahrekan. With regards to different stressor factors in the Persian Gulf, the goal of this study is to assess the ecological status of Bahrekan Bay. It is necessary for the prevention of future probable risks. We used macrobenthose diversity as indicators of ecological status.

MATERIALS AND METHODS The Bahrekan Bay is located 15 km from Hendijan town, in the northwest of the Persian Gulf in Iran. The study site is located in the western part of an important fishery wharf. Fifteen sampling sites were established along the Bay (49° 42' 300" ­ 49° 46' 232"N, 30° 03' 140" - 30° 05' 556" E).Fig 1. Data were obtained from 15 stations (five transect- three stations were located in each transect) from November 2008 to August 2009 in the middle of each season. The stations 1, 4, 7, 10 and 13 were located near the shoreline. Physicochemical parameters of sea water such as salinity (PSU),

temperature (° C), dissolved oxygen (mg/l), pH (units) and conductivity (µs) were determined in all seasons using Hydrolab multimeter (HORIBA, U10). Samples were collected using a Vanveen grab (0.025 m2) taking four replicates at each station. 3 replicates for macrobenthose analysis and 1 sample with three replicates for grain size and total organic matter of the sediment were considered. Macrobenthose samples were sieved on a board with a 0.5 mm mesh size, preserved in 5% formalin solution in sea water and then transferred to the laboratory. The samples were preserved in 99% ethanol and then transferred into 1 g/l of Rose Bengal solution stain for identification (Holme and McIntyre, 1984). Benthic species were sorted under a dissecting microscope using 16× magnification and all macroinvertebrates were identified to the lowest possible taxonomic level, often to family level, by use of systematic and classification keys (Ponder et al., 2000; Martin and Davis, 2001; Glasby and Fauchald, 2002). Previous studies have shown that this level of taxonomic resolution is cost-effective and is sufficient for detecting effects associated with a variety of anthropogenic disturbances (Warwick, 1993; James et al., 1995; Chapman, 1998). In order to determine distribution of sediment particle size, the first part of each sample was dried at 70°C for 48 h and sieved through a nested series of sieves. The other part of each sample was first dried at 70°C for 48 h and then combusted at 550°C for 60 min to determine the total organic matter content through weight loss (ROPME, 1999). Benthic indices include the routine indices of species diversity, the Shannon­Wiener diversity index, the Simpson diversity index, the Brilluin and N1 diversity indices and the evenness indices. Diversity species indices were calculated on the 0.025 m2 sampling surface, and then the average of 3 times sampling was computed in all stations. The calculation of diversity indices was done using ecological methodology software version 6.0 that contain different programs for calculating different indices and variables (Krebs, 2001). Data analysis were made using the Statistical Package for the Social Sciences (SPSS) version 13.

RESULTS The measured results of physico-chemical parameters of water are shown in Table 1. Based on statistical analysis, there were significant differences between physicochemical parameters of water in all seasons (P < 0.05) except pH. There were no significant differences between pH in winter and spring (P > 0.05). The results of physicochemical parameters during four seasons showed little fluctuations (P > 0.05). In addition, changes in the diversity of benthic communities could not be explained based on physico-chemical parameters of water except dissolved oxygen (DO). The higher diversity was obtained

Figure 1.The location of sampling stations in Bahrekan Bay (Northwest of Persian gulf).

in winter with a higher level of DO. The variations of all parameters are shown in Figure 2. The results of the grain size analysis are shown in Table 2. The results showed that more than 98% of the grain size of the sediment in all stations in autumn, winter and summer were <0.063 mm and in spring more than

91% of the grain size of the sediment were <0.063 mm. Hence, the sediment of this region can be categorized as clay. Based on statistical analysis, there were significant differences between the grain sizes of sediment in spring with the grain size of sediment in other seasons (P < 0.05). On the other hand, there were no significant

Table 1. Seasonal mean of physico-chemical parameters of sea water.

Season Autumn Winter Spring Summer Total

T(° C) Mean ±SEM a 18.66±0.07 16.04±0.03b 25.64±0.02c 30.38±0.01d 22.67±0.74

DO(mg/L) Mean ±SEM a 5.94±0.03 8.15±0.03b 5.63±0.01c 4.84±0.01d 6.14±0.16

Salinity (PSU) Mean ±SEM a 53.51±0.21 49.84±0.11b 45.31±0.08c 40.46±0.11d 47.28±0.64

pH (units) Mean ±SEM a 8.5±0.005 8.44±0.01b 8.42±0.00b 8.34±0.00d 8.42±0.08

EC(µs) Mean ±SEM a 66.55±0.13 68.13±0.07b 68.69±0.03c 70.02±0.06d 68.35±0.17

Different superscripts within the same column are significantly different at P < 0.05.

80 Physico-chemical parameters 70 60 50 40 30 20 10 0 Autumn Winter Season

Figure 2. Comparison of physico-chemical parameters of water in different seasons in Bahrekan Bay (autumn 2008 - summer 2009).

Temperature Salinity DO PH EC

Spring

Summer

Table 2. Seasonal mean of sediments grain size percentage analysis.

Season Autumn Winter Spring Summer Total

%Clay Mean ± SD 98.34±1.09abd 98.41±1.16abd 91.38±5.66c 98.08±2.04abd 96.56±4.27

%Silt Mean ± SD 0.68±0.41abd 0.64±0.40abd 1.20±0.34c 0.67±0.48abd 0.80±0.47

%Sand Mean ± SD 0.97±0.95abd 1.20±1.56abd 6.98±6.00c 1.22±1.95abd 2.59±4.10

Different superscripts within the same column are significantly different at P < 0.05.

differences between the grain size of sediment in autumn, winter and summer (P > 0.05). Also, there were negative correlations between percentage silt and percentage total organic matter (TOM) in winter. In addition, significant positive correlations between percentage clay and percentage TOM were observed in spring and

significant negative correlations between percentage sand and percentage TOM were also observed in spring. The results of the total organic matter of sediment analysis are shown in Table 3. The highest mean of percentage TOM was obtained in autumn and the lowest obtained in summer. According to statistical analysis, there were significant differences between percentage TOM of sediment in autumn and winter with percentage TOM of sediment in other seasons (P < 0.05), but there were no significant differences between percentage TOM of sediment in spring and summer (P > 0.05). The amount of percentage TOM in each season showed no significant variation between stations (P > 0.05). In spring, significant negative correlation between percentage TOM and sand and significant positive correlation between percentage TOM and clay were observed. The average diversity indices of macrobenthos obtained in different seasons are shown in Table 4. The results showed that the highest diversity was related to winter and the lowest diversity was related to autumn. In this study, four indices for evaluation and comparison of

Table 3. Seasonal mean of sediments TOM percentage

Parameter Mean% ± SEM

Autumn 36.39±0.75a

Winter 24.34±0.63b

Spring 21.24±0.54c

Summer 19.01±0.51c

Total 25.25±0.99

Different superscripts within the same row are significantly different at P < 0.05.

Table 4. Seasonal mean of diversity indices.

Season Autumn Winter Spring Summer Total

Simpson Mean ± SEM 0.16±0.01a 0.13±0.01a 0.14±0.01a a 0.15±0.08 0.14±0.04

Shanon Mean ± SEM 3.17±0.06a 3.45±0.06b 3.41±0.05ab ab 3.40±0.07 3.36±0.03

Brilluin Mean ± SEM 2.91±0.07a 3.17±0.05b 3.13±0.05ab ab 3.13±0.06 3.09±0.031

N1 Mean ± SEM 9.38±0.38a 11.44±0.42b 11.01±0.42ab ab 11.05±0.55 10.71±0.23

Simpson,E Mean ± SEM 0.41±0.02a 0.35±0.01bc 0.37±0.01abc d 0.30±0.10 0.35±0.08

Camargo,E Mean ± SEM 0.43±0.01abc 0.40±0.01abcd 0.43±0.01abc d 0.36±0.08 0.40±0.06

Different superscripts within the same column are significantly different at P < 0.05.

14 12 10 Index 8 6 4 2 0 Autumn Winter Season

Figure 3. Comparison of diversity indices mean in different seasons in Bahrekan Bay (autumn 2008 - summer 2009).

Simpson Shanon Brillouin N1

Spring

Summer

diversity species and two indices for evenness of species were used. Simpson's diversity index ranged from 0 (high diversity) to 1 (low diversity). A healthy benthic macroinvertebrate community should have a lower Simpson's diversity index. Shannon-Wiener diversity index measures the amount of order in the community by using the number of species and the number of individuals in each species. The value increases with the number of species in the community. A healthy benthic macroinvertebrate community should have a higher Shannon-Wiener diversity index. According to the statistical analysis (Table 4), there were no significant differences between mean of Simpson index in all seasons (P > 0.05). There were significant differences between Shanon index in autumn and winter (P < 0.05). The statistical analysis for Brilluin and N1 indices were the same as Shanon index. There

were significant differences between Simpson, E index in autumn, winter and summer (P < 0.05). There were significant differences between Camargo, E index in summer with Camargo, E index in autumn and winter (P < 0.05). Figures 4 - 7 shows that four calculated indices can be used for presenting species diversity in the study area. But with regards to the variations of N1 index compared to Shanon and Brilliun indices (Figures 4 - 7), it can be stated that among stations where diversity has little fluctuations based on N1 index, the degree of fluctuations is more recognizable. Evenness index measures the evenness or equitability of the community by scaling one of the heterogeneity measures relative to its maximal value that each specie in the sample is represented by the same number of individuals. Evenness index ranges from 0 (low equitability) to 1 (high equitability). The mean

16 14 12 10 Index 8 6 4 2 0 1 2 3 4 5 6 7 8 Station

Figure 4. Comparison of macrobenthose diversity indices of all stations in Bahrekan bay (autumn 2008).

Shanon N1 Brillouin Simpson

9

10

11

12

13

14

15

18 16 14 12 Index 10 8 6 4 2 0 1 2 3 4 5 6 7 8 Station

Figure 5. Comparison of macrobenthose diversity indices of all stations in Bahrekan Bay (winter 2008).

Shanon N1 Brillouin Simpson

9

10

11

12

13

14

15

results of evenness indices were between 0.35 and 0.40. It is understood that, equitability of macrobenthic community is not very high. This is in agreement with the results of species diversity indices. DISCUSSION In this study, the results of diversity indices indicated that macrobenthose in Bahrekan Bay have a good variation and it was concluded that there is an ecological equilibrium in the stations which is similar to the results of Havizavi (2009). The results of the present study showed that macrobenthose diversity can be used as a good indicator for evaluating the ecological status which is similar to the results of Dehghan (2007), Havizavi (2009)

and Anbuchezhian et al. (2009). In this study, annual mean of Simpson index was 0.14 ± 0.04 which indicates that macrobenthose in Bahrekan Bay has good variations. The results of Shanon­Wiener, Brilluin and N1 (number of equally common species) indices confirm the results of Simpson index (Figures 4 - 7). According to the Welch pattern, the annual mean of Shanon index was 3.36 which evaluates the unpolluted status in the study area regarding Welch pattern (1992) in which H´ > 3 represents unpolluted regions, H´ < 1 represents polluted status and 1 < H´ < 3 represents moderate pollution status. For some stations which were located near the shoreline, Shanon indexes 2.4 - 2.9 were obtained which represents the moderate pollution. In stations where diversity had little fluctuations based on N1 index, the degree of the fluctuations were more recognizable. From

20 18 16 14 Index 12 10 8 6 4 2 0 1 2 3 4 5 6 7 8 Station

Figure 6. Comparison of macrobenthose diversity indices of all stations in Bahrekan Bay (spring 2009).

Shanon N1 Brillouin Simpson

9

10

11

12

13

14

15

20 18 16 14 12 10 8 6 4 2 0 1 2 3 4 5 6 7 8 Station 9 10 11 12 13 14 15

Index

Shanon N1 Brillouin Simpson

Figure 7. Comparison of macrobenthose diversity indices of all stations in Bahrekan bay (summer 2009).

Figures 4 ­ 7, it can be stated that the diversity in the stations located near the shoreline is lower than the diversity in the stations located far from the shoreline in all seasons. The stations which were located near the shoreline were affected more by fishing activities. The diversity of macrobenthose was highest in winter and lowest in autumn which is similar to other studies (Havizavi, 2009; Dehghan, 2007). Using these indices is in agreement with the studies of Salas et al. (2004). The effect of environmental parameters such as physiochemical parameters of sea water, grain size and percentage TOM of sediments on diversity species is significant and has been reported in many similar studies (Boesch and Rosenberg, 1981; Muxika et al., 2005; Joydas and Damodaran, 2009). On the other hand, based on the results of the present study, it can be stated

that environmental parameters and their changes are important factors which can closely affect the diversity of species and this meets the findings of previous studies (James et al., 1995; Chapman, 1998; Anbuchezhian et al., 2009). The results revealed negative significant correlations between species diversity and species evenness. Organic matters of sediment were strongly affected by particle size (Milliman, 1994) which is often a function of hydrodynamic regime. Generally, percentage TOM of sediments in aquatic ecosystems has both natural and anthropogenic sources. Our study showed that the high concentrations of organic matters in sediment (ranging from 19.01 - 36.39) could be associated with natural sources because variations of macrobenthose were acceptable. Changes in percentage TOM were related to

environmental variables in different seasons (Nabavi, 1992; Anbuchezhian et al., 2009). The results of high amounts of percentage TOM of sediment are similar to many studies done in the Persian Gulf (Nabavi, 1992; Dehghan, 2007). The results of grain size analysis categorized the region as clay or muddy flat (Nabavi, 1992). Based on the results, the grain size of sediment can be considered as a dominant limiting factor with regards to the diversity of benthic fauna because signi-ficant negative relationships between sediment size (<0.063 µm) with diversity species (P = 0.05) were observed. Benthic communities' diversity was affected by different natural and anthropogenic factors. Physical disturbances are the most important impacts which can decrease the benthic diversity in the study area (Muxika et al., 2005). Fishing activities must be considered as a physical disturbance which can affect the diversity of species. The results of diversity indices (Figures 4 - 7) confirm the reduction in diversity of species in stations which were located near the shoreline and it is due to the considerable fishing activities. The adverse effects of commercial fishing on marine habitat illustrated that the diverse species is closely related to anthropogenic disturbances. Fishing constitutes one of the most significant threats to marine biodiversity. It may also reduce the structural complexity of habitats or change competition and predation among the organisms (Simon et al., 2002). Disturbance in sediment can affect the diversity and assemblage of macrobenthose. However, the potential restructuring to the ecological function of seafloor communities and ecosystems must be considered (Simon and Paul, 2002). Generally, the existence of oil platforms in sea can cause several environmental effects on benthic community such as discharge of drilling mud, production of turbulence, change in grain size and change in benthic communities (Simon, 1992). Based on the results of the present study, it can be stated that the effect of oil platform of the area on diversity of species can be ignored because the diversity of macrobenthic community in the area was acceptable. But, there was negative correlation between macrobenthose diversity and heavy metal concentration. This finding is in agreement with the studies of Chen et al. (2010). Their study have clearly shown the effect of heavy metals on macrobenthic diversity and recorded high diversity and abundance of macrobenthos in areas with low heavy metal concentration. Nevertheless, monitoring programs should be continued to assess the effect of fishing activities and effects of heavy metals on the benthic community. Also, monitoring should be continued to confirm this variations and to ensure that the influence of the fishing activities on the benthic community is temporary or permanent. Therefore, it can be concluded that the study area have high biological potential and monitoring programs should be continued for prevention of future pollutions and disturbances. Conclusively, the use of different indices is highly recommended in determining the environmental quality of a marine system.

ACKNOWLEDGEMENTS The authors wish to appreciate Dr. Ebrahim Rajab zadeh and Mr. Pedram Jafari Shalkouhi for their sincere assistance.

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