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Bu-Olayan A. H, Thomas B. V. Effects Of Trace Metals, Harmful Algal Blooms, Nutrients And Hydrological Variables To Mullet (Liza Klunzingeri) In Kuwait Bay. Biosci Biotechnol Res Asia 2003;2(1)
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Effects Of Trace Metals, Harmful Algal Blooms, Nutrients And Hydrological Variables To Mullet (Liza Klunzingeri) In Kuwait Bay

A. H. Bu-Olayan and B. V. Thomas

POB 5969, Department of Chemistry, Kuwait University, Safat - 13060 (Kuwait).

ABSTRACT: A catastrophic ‘fish kill’ took place in Kuwait Bay between 1999 and 2000, specifically to mullet, Liza klunzingeri. Its recurrence in the consecutive years in low profile only in the Bay region and not elsewhere along the Kuwait Coast stimulated us to investigate the causative factors in five important sites of Kuwait Bay. Among various Harmful Algal Blooms (HABs), Dinophysis caudata was found predominant in the five sites of the Bay. Trace metal levels in seawater, HABs and L. klunzingeri were higher (8.11 ?g l-1, 45.14 ?g g-1and 67.81 ?g g-1, respectively) during HABs enrichment than during their absence (6.11?g l-1 40.29?g g-1 67.41?g g-1, respectively). Observations revealed high mortality of this species due to high trace metals with low nutrient levels (Phosphate, Nitrate and Silicate), and high ammonia levels during high HABs enrichment. Further, high temperature, turbidity and low dissolved oxygen were found to enhance the HABs in the Bay. These variations can be attributed to pollution from wastewater discharges, anthropogenic sources, rapid industrialization and human activities in the Bay. Furthermore, such ‘fish kills’ may not only recur in the near future but are anticipated to cause (1) direct and indirect harmful effects to fish consumers, in man and (2) economical loss from fishing industry, and hence the investigation.

KEYWORDS: Trace metals; HABs; L. klunzingeri; Kuwait Bay

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Bu-Olayan A. H, Thomas B. V. Effects Of Trace Metals, Harmful Algal Blooms, Nutrients And Hydrological Variables To Mullet (Liza Klunzingeri) In Kuwait Bay. Biosci Biotechnol Res Asia 2003;2(1)

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Bu-Olayan A. H, Thomas B. V. Effects Of Trace Metals, Harmful Algal Blooms, Nutrients And Hydrological Variables To Mullet (Liza Klunzingeri) In Kuwait Bay. Biosci Biotechnol Res Asia 2003;2(1). Available from: https://www.biotech-asia.org/?p=3409

Introduction

The first massive outbreak of a HAB that led to “Fish Kills’, particularly of the mullet,Liza klunzingeri (‘Maid fish’), was reported in Kuwait Bay, during the year 19991. Lists on few phytoplankton species (inclusive of oil and trace metal indicator species)2 were found to support evidences to the species listed in five coastal areas of Kuwait Bay3. However, during the year 1999, most of the phytoplankton was found dominated by HABs species such as Dinophysis caudata, D. norvegica (a diorrhetic shell fish poisoning-DSP), Protoperidinium spp., Peridinium spp., and Gymnodinium spp., in the Kuwait Bay. Earlier studies revealed increased trace metal levels in seawater due to anthropogenic inputs, seasonal influences and low photosynthetic activity4-5. The relationship between nutrient depletion during summer and the enrichment of HABs was observed6. The hydrological variables that influence the blooms of six species of red tide flagellates in Osaka Bay was described earlier7. Along with these studies, high temperature and pH leading to the formation of free ammonium in seawater were also reported8. The HABs are anticipated to recur in the future, during favorable conditions in the Kuwait marine ecosystem. Hence, a baseline study was made to determine (a) the effects of trace metals levels in seawater, HABs, phytoplankton and L. klunzingeri, (b) nutrients levels and hydrological variables from five sites of Kuwait Bay that exacerbate marine pollution problems and (c) if dominating HABs such as D. caudata are specifically linked to mass mortality of L. klunzingeri.

Materials and Methods

Five sites, namely Subiyah, Umm-Al-Nammil Is. near Doha, Khadma, Kuwait Tower and Salmiya in Kuwait Bay (Sites I-V in Fig.1), affected by ‘maid fish kill’ were selected for the present study. A mechanized boat with a towing speed maintained at 0.3m s-1 was employed to collect samples by (a) using phytoplankton net of 5mm mesh size, (b) Vandorn water sampler and (c) trawl net for mullet fish. Based on the densities of HABs, samples were labeled “HABs” and “non- HABs” respectively.

Determination of trace metals in seawater Trace metals, Cu, Zn, Fe, Pb and Ni, in seawater that were found (i) significant to marine pollution in the Kuwait Bay3 and (ii) within the detectable limits of Atomic Absorption Spectrophotometer (AAS) were chosen for the present study. Two-liter seawater samples collected from Kuwait Bay sites (I-V) were filtered in a 0.45mm membrane filter. One-liter were amended with 25 ml ammonium-pyrrolidine-dithiocarbonate (APDC-2% v/v), 10mL HCl (0.5 M) and 35mL methyl isobutyl ketone (MIBK-99.5%) in a separatory funnel, shaken for 2 minutes and left undisturbed for 15-20 minutes. Two separate phases, namely, upper and lower solutions (A & B) were obtained. To one liter of fresh seawater, the upper solution (A) was added with APDC, HCl and MIBK and the process was repeated. In another separatory funnel, the lower solution (B) was amended with the above chemicals and eluted. The upper solutions from both A and B were collected in a 50mL volumetric flask and the lower solutions discarded. The upper solutions were analyzed in AAS and the concentration of trace metals measured. Quality measures were followed9.

Table 1 : Metal-wise statistical analysis in seawater, HABs, phytoplankton and ‘Maid fish’ collected during HABs and non-HABs enrichment in Kuwait Bay

Metals Mean S.D. Range Tests Pearson’s t-value/*
          description correlation (r) significance
1. Seawater – during HABs        
Cu 2.40 ±0.26 2.02-2.84 1. Vs 2. 0.99 2.67*
Zn 3.98 ±1.15 2.31-5.72 1. Vs 3. 0.92  
Fe 5.47 ±1.58 3.71-8.11 1. Vs 4. 0.93  
Ni 0.15 ±0.08 0.05-0.31 1. Vs 5. 0.90  
Pb 2.40 ±0.42 1.95-3.14 1. Vs 6. 0.90  
2. Seawater –during non-HABs      
Cu 2.11 ± 0.08 1. 98-2.25 2. Vs 2.  
Zn 3.35 ± 1.05 2.15-4.62 2. Vs 3. 0.91  
Fe 4.12 ± 1.07 2.89-6.11 2. Vs 4. 0.92  
Ni 0.07 ± 0.06 0.01-0.19 2. Vs 5. 0.86  
Pb 1.87 ± 0.63 1.12-3.02 2. Vs 6. 0.86  
3. HABs            
Cu 19.92 ±16.36 0.54-36.87 3. Vs 2. 0.91  
Zn 22.42 ±11.33 5.10-32.84 3. Vs 3.  
Fe 30.77 ±14.83 9.41-45.14 3. Vs 4. 0.99 14.87*
Ni 11.25 ± 6.92 2.54-19.75 3. Vs 5. 0.94  
Pb 12.93 ± 9.96 0.85-29.87 3. Vs 6. 0.94  
4. Non-HABs –(Phytoplankton)      
Cu 16.01 ±13.22 0.45-31.12 4. Vs 2. 0.92  
Zn 18.77 ±11.66 2.59-31.11 4. Vs 3. 0.99  
Fe 27.16 ±13.68 8.15-40.29 4. Vs 4.  
Ni 8.15 ± 5.42 1. 56-15.46 4. Vs 5. 0.95  
Pb 9.84 ± 6.66 0. 41-18.91 4. Vs 6. 0.95  
5. Maid fish- during HABs        
Cu 7.90 ±0.10 7.77-8.02 5. Vs 2. 0.86  
Zn 32.93 ±0.86 31.91-33.79 5. Vs 3. 0.94  
Fe 66.64 ±1.00 65.48-67.81 5. Vs 4. 0.95  
Ni 1.44 ±0.13 1.32-1.62 5. Vs 5.  
Pb 2.74 ±0.16 2.54-2.93 5. Vs 6. 1.00 2.47*
6. Maid fish- during non-HABs        
Cu 7.74 ±0.21 7.48-7.95 6. Vs 2. 0.86  
Zn 32.18 ±1.17 30.98-33.68 6. Vs 3. 0.94  
Fe 66.12 ±1.04 65.12-67.41 6. Vs 4. 0.95  
Ni 1.32 ±0.14 1.21-1.54 6. Vs 5. 1.00  
Pb 2.66 ±0.18 2.49-2.86 6. Vs 6.  

Table 2 : Station-wise statistical analyses in seawater, HABs, phytoplankton and Maid fish during HABs and non-HABs enrichment in Kuwait Bay

Stations Mean S.D. Range Tests Pearson’s t-value/*
        description correlation (r) significance
1. Seawater – during HABs        
Subiyah 2.09 ±1.24 0.05-3.84 1. Vs 2. 0.99 6.63*
Khadma 2.40 ±1.44 0.05-4.13 1. Vs 3. 0.93  
Doha 3.92 ±2.72 0.29-8.11 1. Vs 4. 0.93  
Tower 2.83 ±1.89 0.09-5.48 1. Vs 5. 0.95  
Salmiya 3.15 ±2.19 0.15-6.59 1. Vs 6. 0.95  
2. Seawater –during non-HABs      
Subiyah 1.79 ±1.04 0.01-3.15 2. Vs 2.  
Khadma 1.86 ±1.07 0.02-3.22 2. Vs 3. 0.92  
Doha 3.07 ±2.07 0.16-6.11 2. Vs 4. 0.92  
Tower 2.22 ±1.64 0.02-4.26 2. Vs 5. 0.96  
Salmiya 2.51 ±1.67 0.11-4.68 2. Vs 6. 0.97  
3. HABs            
Subiyah 3.74 ±3.49 0.54-9.62 3. Vs 2. 0.92  
Khadma 9.50 ±6.97 2.48-19.62 3. Vs 3.  
Doha 32.30 ±8.84 18.6-44.81 3. Vs 4. 1.00 3.76*
Tower 23.38 ±8.54 13.9-35.18 3. Vs 5. 0.82  
Salmiya 28.35 ±12.35 14.1-40.29 3. Vs 6. 0.82  
4. Non-HAB’s –(Phytoplankton)      
Subiyah 2.94 ±3.08 0.41-8.19 4. Vs 2. 0.92  
Khadma 7.68 ±5.78 2.12-16.10 4. Vs 3. 1.00  
Doha 26.86 ±9.81 14.1-40.29 4. Vs 4.  
Tower 19.81 ±8.65 9.86-32.12 4. Vs 5. 0.81  
Salmiya 23.64 ±10.8 11.1-40.28 4. Vs 6. 0.82  
5. Maid fish- during HABs        
Umm-al       5. Vs 2. 0.96  
Nammil       5. Vs 3. 0.82  
Is. (site       5. Vs 4. 0.81  
near       5. Vs 5.  
Doha) 11.43 ±4.53 6.73-18.21 5. Vs 6. 1.00 2.91*
6. Maid fish- during non-HABs        
Umm-al       6. Vs 2. 0.97  
Nammil       6. Vs 3. 0.82  
Is. (site       6. Vs 4. 0.82  
near       6. Vs 5. 1.00  
Doha) 10.59 ±4.35 5.55-16.32 6. Vs 6.  

Mean & Range in (ìg l-1) for seawater and (ìg g-1) for other samples; S.D.: Standard Deviation; HABs: dominated by Dinophysis sp., Protoperidium sp., and Peridinum sp.; Phytoplankton: dominated by diatoms, non-HABs dinoflagellates, *significant at P <0.05.

Phytoplankton analysis

Phytoplankton samples (75ml) were collected at a depth of 0.1m from the surface in sterile plastic bottles. Sub-samples (25ml) were fixed in Lugol’s solution for identification of species. Sub samples were further diluted to 5ml based on plankton density. HABs causing phytoplankton were identified and counted as described10. The remaining phytoplankton (50ml) filtered by 0.5ìm Whatman filter paper was placed in a sterile petridish and dried in an oven at 40oC for 12hrs. Dried phytoplankton weighing 0.023g (constant), was pre-digested separately in 6% Nitric acid (v/v) and 4% HCl (v/v) for 48 hrs in a 50ml Fisher brand disposable sterile centrifuge tube9. The samples were diluted to 50ml in de-ionized distilled water and digested in an automatic microwave digester (SpectroPrep-CEM) and the metal content (ìg/g) read in the AAS. The accuracy of the method was verified using a Standard Reference Material (SRM-1547-Peach leaves) from the National Bureau of Standards. The average recoveries (%) of all the trace metal levels were 94.20 ±0.07.

Trace metals in L. klunzingeri

klunzingeri was collected from the Umm-al Nammil Island located near Doha (site III) in Kuwait Bay. This island was found (1) easily accessible to fish collection from traditional fish trap called ‘Hadrah’, (2) prone to varied hydrological fluctuations and (3) the center point among the five sites of the Bay. Using non-contaminating laboratory measures, their body tissues (10g) were dried in a hot air oven (Gallen Camp II) at 50oC for 48 hrs. They were ground to <250mm size and packed in sterile polyethylene containers. Sample analysis on ground powder (2g) was carried out as described for phytoplankton. The accuracy of the method was verified by Certified Reference material: Dogfish muscle (DORM-2) from the National Bureau of Standards. The average recoveries (%) of all the trace metal levels were 95.61 ±0.06.

Figure 1 : Kuwait Bay sites of the Arabian Gulf Figure 1 : Kuwait Bay sites of the Arabian Gulf

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Determination of nutrients in seawater

The samples for nutrients analyses such as phosphate and silicate in seawater were pretreated for chloride interferences as described9 and estimated by spectroscopy method with absorbencies measured at 880 and 810nm, respectively11-12. In the case of nitrate, the potential measurement of NO3-N concentration standards and samples were recorded against a semi-logarithmic graph with a slope of +57 ± 3 mV/decade at 25oC and concentrations measured from the calibration curve13.

Hydrological variables

Hydrological variables like pH, salinity, dissolved-oxygen, temperature and turbidity were checked using a multi-sensor array, Horiba (U-10), Int. Inc., USA. The methodologies of 9,14 were adopted to analyze ammonium level in the samples.

Results and Discussion

Trace metals were in the sequence of Fe>Zn>Cu>Pb and Ni, in L. klunzingeri, seawater, and phytoplankton (diatoms) collected from the five sites off the Kuwait Bay. L.klunzingeri was found to be susceptible during HABs outbreak among other fish in the Kuwait Bay. This may be attributed to its

highly sensitivity to pollutants and varying hydrological variables. Trace metals levels was found relatively high in all the samples in Site-IV followed by Sites III>I>II>V in the presence of HABs. However, in their absence trace metal levels followed a sequence of Sites III>IV>V>II>I.

Figure 2 : Station wise nutrient levels in seawater during HABs and Non-HABs Figure 2 : Station wise nutrient levels in seawater during HABs and Non-HABs

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Table 3: Mean hydrological parameters in seawater during HABs and non-HAB off the Kuwait Bay

    (HAB)       (Non-HAB)  
Stations pH Tem. Sal. DO Tb. pH Tem. Sal. DO Tb.
    (oC) (‰) (mg l-1)     (oC) (‰) (mg l-1)  
Subiyah-I 8.2 30 35 3.3 5 8.1 27 34 4.1 6
Khadma-II 8.1 29 34 3.5 2 8.1 26 36 3.8 2
Doha-III &                    
UmmAl-                    
Nammil Is. 8.2 30 36 3.4 2 8.2 28 38 4.4 3
K.Tower-IV 8.2 31 36 3.5 1 8.2 29 35 4.4 3
Salmiya-V 8.1 31 37 3.6 2 8.2 29 36 4.3 3

Table 4 : Comparative analysis on the trace metals levels in seawater, HABs, phytoplankton, fish and nutrients in other parts of the globe

Description Seawater HABs   Phytoplankton ‘Maid’ Fish References
  concentration concentration concentration concentration
  (µg l -1) (µg g -1) (µg g -1)   (µg g -1)    
Trace metals                
Cu 0.45-3.86 2.80-38.73 5-59.17   6.40-7.80 1,2,5
  2.02-2.84 0.54-36.87 0.45-31.12 7.48-8.02 Present Study
Fe 4.12-9.90 5.60-42.55 4.90-126.8 49.50-66.90 2,3,5
  3.71-8.11 9.41-44.81 8.15-40.29 30.98-33.79 Present Study
Zn 0.54-9.90 2.84-40.76 10.40-210 7.60-32.20 1,2,5
  2.31-5.72 5.10-32.84 4.01-31.11 65.12-67.81 Present Study
Ni 0.18-2.80 ND   2.45-41.01 1.50-1.60 1,2,5
  0.05-0.31 2.54-19.75 1.56-15.46 1.21-1.62 Present Study
Pb 0.03-12.2 0.05-32.50 4.73-209   0.20-2.80 1,2,5
  1.95-3.14 0.85-29.87 0.41-18.91 2.49-2.93 Present Study
Nutrients                
Phosphate 0.01-0.30 ND   ND   ND   4,5
  0.01-0.04 N D   N D   N D   Present Study
Silicate 0.15-0.85 ND   ND   ND   4,5
  0.12-0.81 N D   N D   N D   Present Study
Nitrate 0.02-0.55 ND   ND   ND   4,5
  0.02-0.69 N D   N D   N D   Present Study

Trace metals in seawater

Trace metals were high in seawater during the occurrence of HABs enrichment than during its presence in very low densities irrespective of the sampling sites. This may be attributed to: (1) the discharge of domestic sewage outfall from Shuwaikh, an adjoining industrial area, (2) chemical effluent discharge from the nearby desalination plant and wastewater treatment plant from Shuwaikh area, (3) synergistic effects of density-stratified water column, low water current action, low utility of trace metals in seawater by the existing phytoplankton due to low photosynthetic activity or death of primary producers 4-5. Further, t-tests revealed significant difference to trace metals in seawater analyzed during HABs than in their absence (Tables 1 and 2) and supports the earlier investigation3.

HAB’s abundance, phytoplankton and trace metal levels

Enrichment of HAB especially D. caudata displacing other phytoplankton was noted just before the onset of summer and winter in Kuwait Bay (sites: I-V). Site-I recorded the first observation of D. caudata. HABs spread to sites II-IV soon after their enrichment for a short period (within a week’s time) from site-I. This may be attributed to the one way-directional flow of water current from the Shatt-al-Arab River, originating from Iraq to the North of Kuwait3. In the present study, trace metals were found high in D. caudata than in phytoplankton (harmless diatoms and dinoflagellates), attributing to: (1) favorable hydrological parameters like temperature, pH and salinity and (2) human activities in the five sites and (3) sewage and effluent disposals into the Bay. The significance of this observation was also confirmed statistically (Table 2).

Trace metals in L. klunzingeri

‘Fish kill’ to the tune of 2MT occurred first, in the year 1999 and reoccurred in the following year in an un-quantifiable measure, especially in Kuwait Bay (sites III-V)1. Relatively, high trace metals level was found significant during peak HABs enrichment (Table 2). Among the HABs, the most abundant species Dinophysis caudata, could be attributed to their indirect action to the ‘fish kill’, as their abundance was found to alter the dissolved oxygen at relatively high temperature in the Bay sites. Further, trace metals and site-wise Pearson’s correlation revealed significant difference between seawater, HAB, phytoplankton and ‘maid fish’ (Tables 1 and 2). It is also interesting to observe that no other fish other than the ‘maid fish’, reported such high mortality in Kuwait Bay. Thus, the occurrence of HABs (D. caudata) could be used as an indicator species to ‘fish kill’.

Nutrients in seawater

Nutrients were in the sequence of Silicate>Nitrate>Phosphate irrespective of seasons and sites. Mean nutrient levels were lower (Silicate: 0.15-0.58; Nitrate: 0.6-0.44; Phosphate: 0.01-0.03) during HABs enrichment than in the latter’s absence (Silicate: 0.40-0.571; Nitrate: 0.9-0.55; Phosphate: 0.01-0.03), (Fig.2). This may be attributed to (1) the utility of nutrients from the marine environment by the HABs, (2) depletion of nutrient resources, a view that supports the earlier observation6, (3) temperature stratification and (4) flow rate of water current in the Bay. However, in an overall view, the nutrient levels were observed lower than the earlier studies in Kuwaiti waters (Table 4).

Ammonia level was found relatively high during HABs enrichment than in their absence in this Bay when compared to the earlier studies (Fig.2) 8. Acute ammonia toxicity with increasing temperature and low dissolved oxygen was reported by earlier workers14. This phenomenon was observed in the present findings during HAB enrichment and hence attributed to be one among the cause for ‘fish kill’ in this Bay.

Hydrological variables

Few environmental manipulations by human activities and HAB outbreak over recent years have been found to alter the hydrological features in the five sites of Kuwait Bay when compared to the earlier studies3. An interesting observation in the present study was that of the HABs abundance during high temperature (Table 3). This supported the other views 7. This alteration of temperature in seawater could be attributed to (1) direct pumping of untreated sewage and effluents into the Bay and (2) warm water discharge from the power and thermal plants located in Subiyah region (Site I).

Conclusion

Both observations and statistical analysis supports the effects of (1) high trace metals pollution in the Bay that finds its pathway from various sources, (2) temporary replacement of D. caudata abundance (HABs) over other phytoplankton species (non-HABs) due to water current, biophysical and hydro-chemical factors, and the combination of marine pollutants, (3) hydrological alterations in the Bay through desalination, power and thermal plants causing high temperature and low dissolved oxygen, (4) altered nutrient levels and (5) rapid industrialization and recreational activities at the Kuwait Bay anchorage, leading to mass mortality of L. klunzingeri over recent years and label D. caudata as an indicator species to ‘fish kill’ in future studies.

Acknowledgments

We acknowledge Kuwait Foundation for the Advancement of Sciences (KFAS) for their invaluable financial support to the project KFAS 2000-05-02. Thanks extended to Dr. R. Al-Hassan, Dean, Department of Biological Sciences, Science Analytical Facilities (SAF) and Research Administration, Kuwait University for providing us laboratory facilities and sample analyses respectively.

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