Abstract
A biomonitoring study was conducted using some biotic (Pomadasys hasta and Lutjanus russellii fish) and abiotic (water and sediment) components of the Red Sea coast of Hodeida, Yemen Republic along two polluted sites (Al-Dawar beach and Urj village) in comparison to a reference site (Al-Nukhailah beach). The studied fish biomarkers included hepatosomatic index (HSI), condition factor (K), scaled mass index (SMI), catalase, glutathione-S-transferase (GST), malondialdehyde (MDA), total protein and albumin. In addition, metals (Fe, Cu, Zn, Pb and Cd) concentrations in water and sediment were measured and sediment pollution assessment was carried out using contamination factor (CF), geoaccumulation index (Igeo), pollution load index (PLI) and enrichment factor (EF). The studied metals concentration in water and sediment samples showed significant increase among the polluted sites in comparison to the reference site. Sediment pollution assessment generally confirmed that Urj village was the most contaminated site followed by Al-Dawar beach. Catalase, GST and MDA proved to be the most responsive biomarkers with increased values of GST and MDA at sites influenced by agricultural, urban and industrial activities while catalase, HSI, K, SMI, total protein and albumin showed the opposite trend. This study recommends monitoring of sediment Igeo and EF values as well as SMI, catalase, GST and MDA as sensitive indicators of different anthropogenic activities and their effects on aquatic ecosystems under complex and different gradients of metal pollution. In addition, P. hasta proved to be more sensitive towards the detected pollution condition.
Similar content being viewed by others
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Akbal F, Gurel L, Bahadır T, Guler I, Bakan G, Buyukgungor H (2011) Water and sediment quality assessment in the mid-Black Sea coast of Turkey using multivariate statistical techniques. Environ Earth Sci 64(5):1387–1395. doi:10.1007/s12665-011-0963-6
Ali Z, Malik RN, Qadir A (2013) Heavy metals distribution and risk assessment in soils affected by tannery effluents. Chem Ecol 29:1–17. doi:10.1080/02757540.2013.810728
Al-Shiwafi N, Rushdi AI, Ba-Issa A (2005) Trace metals in surface seawaters and sediments from various habitats of the Red Sea coast of Yemen. Environ Geol 48(4–5):590–598. doi:10.1007/s00254-005-1315-1
APHA, American Public Health Association (1998) Standard methods for examination of water and wastewater. American Public Health Association, New York
Atli G, Canli M (2007) Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol Part C: Toxicol Pharmacol 145(2):282–287. doi:10.1016/j.cbpc.2006.12.012
Atli G, Alptekin Ö, Tükel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol Part C Toxicol Pharmacol 143(2):218–224. doi:10.1016/j.cbpc.2006.02.003
Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Adams SM (ed) biological indicators of aquatic ecosystem stress. Am Fish Soc Bethesda, pp 111–148
Bebianno MJ, Geret F, Hoarau P, Serafim MA, Coelho MR, Gnassia-Barelli M, Romeo M (2004) Biomarkers in Ruditapes decussatus: a potential bioindicator species. Biomarkers 9:305–330. doi:10.1080/13547500400017820
Ben Ameur W, de Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64(2):241–251. doi:10.1016/j.marpolbul.2011.11.026
Ben-Khedher S, Jebali J, Kamel N, Banni M, Rameh M, Jrad A, Boussetta H (2013) Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta Lagoon: an integrated approach in biomonitoring of marine complex pollution. Environ Sci Pollut Res 20(4):2616–2631. doi:10.1007/s11356-012-1156-x
Bervoets L, Blust R (2003) Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126:9–19. doi:10.1016/S0269-7491(03)00173-8
Bhatia NP, Sandhu GS, Johal MS (2002) Endosulfan induced changes in blood chemistry of Heteropneustes fossilis. Pollut Res 21(3):323–327
Birch GF, Olmos MA (2008) Sediment-bound heavy metals as indicators of human influence and biological risk in coastal water bodies. ICES J Mar Sci 65:1407–1413. doi:10.1093/icesjms/fsn139
Buat-Menard P, Chesselet R (1979) Variable influence of the atmospheric flux on the trace metal chemistry of oceanic suspended matter. Earth Planet Sci Lett 42:399–411. doi:10.1016/0012-821X(79)90049-9
Buccolieri A, Buccolieri G, Cardellicchio N, Dell’Atti A, Di Leo A, Maci A (2006) Heavy metals in marine sediments of Taranto Gulf (Ionian Sea, Southern Italy). Mar Chem 99:227–235. doi:10.1016/j.marchem.2005.09.009
Chandran R, Sivakuma AA, Mohandas S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica. Comp Biochem Physiol Part C: Toxicol Pharmacol 140(3–4):422–426. doi:10.1016/j.cca.2005.04.007
Coles EH (1986) Veterinary clinical pathology. WB Saunders, Philadelphia, pp 10–42
Deshmukh VM (1973) Fishery and biology of Pomadasys hasta (Bloch). Indian J Fish 20(1–2):497–522
Ergin M, Saydam C, Baştürk Ö, Erdem E, Yörük R (1991) Heavy metal concentrations in surface sediments from the two coastal inlets (Golden Horn Estuary and Izmit Bay) of the northeastern Sea of Marmara. Chem Geol 91:269–285. doi:10.1016/0009-2541(91)90004-B
Esteve C, Alcaide E, Ureña R (2012) The effect of metals on condition and pathologies of European eel (Anguilla anguilla): in situ and laboratory experiments. Aquat Toxicol 109:176–184. doi:10.1016/j.aquatox.2011.10.002
Fonseca VF, França S, Serafim A, Company R, Lopes B, Bebianno MJ, Cabral HN (2011) Multi-biomarker responses to estuarine habitat contamination in three fish species: dicentrarchus labrax, Solea senegalensis and Pomatoschistus microps. Aquat Toxicol 102:216–227. doi:10.1016/j.aquatox.2011.01.018
Gibbons WN, Munkittrick KR (1994) A sentinel monitoring framework for identifying fish population responses to industrial discharges. J Aquat Ecosyst Health 3:227–237. doi:10.1007/BF00043244
Grune T, Jung T, Merker K, Davies K (2004) Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and ‘aggresomes’ during oxidative stress, aging, and disease. Int J Biochem Cell Biol 36(12):2519–2530. doi:10.1016/j.biocel.2004.04.020
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Hakanson LL (1980) An ecological risk index aquatic pollution control, a sedimentological approach. Wat Res 14(8):975–1001. doi:10.1016/0043-1354(80)90143-8
Heath AG (1987) Water pollution and fish physiology. CRC Press Inc, Boca Raton, FL
Heba HM, Al-Edresi MA, Al-Saad HT, Abdelmoneim MA (2004) Background levels of heavy metals in dissolved, particulate phases of water and sediment of Al-Hodeidah Red Sea coast of Yemen. Mar Sci 15:53–71
Jana S, Bandyopadhyaya N (1987) Effect of heavy metals on some biochemical parameters in the freshwater fish, Channa punctatus. Environ Ecol 5(3):488–493
Jebali J, Sabbagh M, Banni M, Kamel N, Ben-Khedher S, M’hamdi N, Boussetta H (2013) Multiple biomarkers of pollution effects in Solea solea fish on the Tunisia coastline. Environ Sci Pollut Res 20:3812–3821. doi:10.1007/s11356-012-1321-2
Karadag H, Fırat Ö, Fırat Ö (2014) Use of oxidative stress biomarkers in Cyprinus carpio L for the evaluation of water pollution in Ataturk Dam Lake (Adiyaman, Turkey). Bull Environ Contam Toxicol 92(3):289–293. doi:10.1007/s00128-013-1187-0
Karbassi AR, Monavari SM, Nabi Bidhendi GR, Nouri J, Nematpour K (2008) Metal pollution assessment of sediment and water in the Shur River. Environ Monit Assess 147(1–3):107–116. doi:10.1007/s10661-007-0102-8
Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5764
Li GG, Hu BQ, Bi JQ, Leng QN, Xiao CQ, Yang ZC (2013) Heavy metals distribution and contamination in surface sediments of the coastal Shandong Peninsula (Yellow Sea). Mar Pollut Bull 76:420–426. doi:10.1016/j.marpolbul.2013.08.032
Li M, Zang S, Xiao H, Wu C (2014) Speciation and distribution characteristics of heavy metals and pollution assessments in the sediments of Nashina Lake, Heilongjiang, China. Ecotoxicol 23:681–688. doi:10.1007/s10646-014-1180-3
Lim WY, Aris AZ, Praveena SM (2012) Application of the chemometric approach to evaluate the spatial variation of water chemistry and the identification of the sources of pollution in Langat River, Malaysia. Arab J Geosci 6(12):4891–4901. doi:10.1007/s12517-012-0756-6
Linde-Arias RA, Inácio FA, de Alburquerque C, Freire MM, Moreira CJ (2008) Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian River. Sci Total Environ 399:186–192. doi:10.1016/j.scitotenv.2008.03.028
Liu J, Wu H, Feng J, Li Z, Lin G (2014) Heavy metal contamination and ecological risk assessments in the sediments and zoobenthos of selected mangrove ecosystems, South China. Catena 119:136–142. doi:10.1016/j.catena.2014.02.009
Maceda-Veiga A, Monroy M, Viscor G, De Sostoa A (2010) Changes in non-specific biomarkers in the Mediterranean barbell (Barbus meridionalis) exposed to sewage effluents in a Mediterranean stream (Catalonia, NE Spain). Aquat Toxicol 100:229–237. doi:10.1016/j.aquatox.2010.07.014
Maceda-Veiga A, Green AJ, De Sostoa A (2014) Scaled body-mass index shows how habitat quality influences the condition of four fish taxa in north-eastern Spain and provides a novel indicator of ecosystem health. Freshw Biol 59:1145–1160. doi:10.1111/fwb.12336
Maggioni T, Hued AC, Monferrán MV, Bonansea RI, Galanti LN, Amé MV (2012) Bioindicators and biomarkers of environmental pollution in the middle-lower basin of the Suquía River (Córdoba, Argentina). Arch Environ Contam Toxicol 63:337–353. doi:10.1007/s00244-012-9785-0
Maines MD, Gibbs PEM (2005) 30 some years of heme oxygenase: from a “molecular wrecking ball” to a “mesmerizing” trigger of cellular events. Biochem Biophys Res Commun 338:568–577. doi:10.1016/j.bbrc.2005.08.121
Marzouk MS, Zaghloul KH, Hanna MI, Mahrous KF (2005) The clinical signs, histopathological and physiological status associated with acute and chronic exposure to Benzo-a-Pyrene in the cultured fish Oreochromis niloticus. J Egy Germ Soc Zool 47:283–312
Mieiro CL, Pacheco M, Pereira ME, Duarte AC (2011) Mercury organotropism in feral European sea bass (Dicentrarchus labrax). Arch Environ Contam Toxicol 61(1):135–143. doi:10.1007/s00244-010-9591-5
Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicol 19(1):105–123. doi:10.1007/s10646-009-0395-1
Morcos SA, Varely D (1990) Physical and chemical oceanography of the Red Sea. Oceanogr Mar Biol Annu Rev 8:73–202
Moyo NAG (2013) An analysis of the chemical and microbiological quality of ground water from boreholes and shallow wells in Zimbabwe. Phys Chem Earth 66:27–32. doi:10.1016/j.pce.2013.06.003
Müller G (1979) Schwermetalle in den Sedimenten des Rheins-Veränderungen seit. Umschau 79:778–783
Ndiaye A, Sanchez W, Durand J, Budzinski H, Palluel O, Diouf K, Ndiaye P, Panfili J (2012) Multiparametric approach for assessing environmental quality variations in West African aquatic ecosystems using the black-chinned tilapia (Sarotherodon melanotheron) as a sentinel species. Environ Sci Pollut Res 19:4133–4147. doi:10.1007/s11356-012-0979-9
Nelson JS (1994) Fishes of the world, 3rd edn. Wiley, New York, p 523
Oliva M, Vicente JJ, Gravato C, Guilhermino L, Galindo-Riaño MD (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotoxicol Environ Saf 75(1):151–162. doi:10.1016/j.ecoenv.2011.08.017
Oliveira M, Ahmad I, Maria VL, Pacheco M, Santos MA (2010) Monitoring pollution of coastal lagoon using Liza aurata kidney oxidative stress and genetic endpoints: an integrated biomarker approach. Ecotoxicol 19:643–653. doi:10.1007/s10646-009-0436-9
Omar WA, Saleh YS, Marie M-AS (2014) Integrating multiple fish biomarkers and risk assessment as indicators of metal pollution along the Red Sea coast of Hodeida, Yemen Republic. Ecotoxicol Environ Saf 110:221–231. doi:10.1016/j.ecoenv.2014.09.004
Osman AG, Al-Awadhi RM, Harabawy ASA, Mahmoud UM (2010) Evaluation of the use of protein electrophoresis of the African catfish Clarias gariepinus (Burchell, 1822) for biomonitoring aquatic pollution. Environ Res 4(3):235–243. doi:10.3923/erj.2010.235.243
Padmini E, Rani MU (2009) Evaluation of oxidative stress biomarkers in hepatocytes of grey mullet inhabiting natural and polluted estuaries. Sci Total Environ 407(15):4533–4541. doi:10.1016/j.scitotenv.2009.04.005
Pampanin DM, Marangon I, Volpato E, Campesan G, Nasci C (2005) Stress biomarkers and alkali-labile phosphate level in mussels (Mytilus galloprovincialis) collected in the urban area of Venice (Venice Lagoon, Italy). Environ Pollut 136(1):103–107. doi:10.1016/j.envpol.2004.12.010
Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. doi:10.1111/j.1600-0706.2009.17643.x
Phiri O, Mumba P, Moyo BH, Kadewa W (2005) Assessment of the impact of industrial effluents on water quality of receiving rivers in urban areas of Malawi. Int J Environ Sci Technol 2(3):237–244. doi:10.1007/BF03325882
Rajeshkumar S, Mini J, Munuswamy N (2013) Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of Milkfish (Chanos chanos) of Kaattuppall Island, Chennai, India. Ecotoxicol Environ Saf 98:8–18. doi:10.1016/j.ecoenv.2013.07.029
Ruas CB, Carvalho CS, De Araújo SS, Espíndola EL, Fernandes MN (2008) Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicol Environ Saf 71(1):86–93. doi:10.1016/j.ecoenv.2007.08.018
Sakai H, Kojima Y, Saito K (1986) Distribution of heavy metals in water and sieved sediments in the Toyohira river. Wat Res 20:559–567. doi:10.1016/0043-1354(86)90019-9
Saleh YS, Marie M-AS (2015) Assessment of metal contamination in water, sediment, and tissues of Arius thalassinus fish from the Red Sea coast of Yemen and the potential human risk assessment. Environ Sci Pollut Res 22:5481–5490. doi:10.1007/s11356-014-3780-0
Satoh K (1978) Serum lipid peroxide in cerebrovascular disorder determined by a new colorimetric method. Clin Chim Acta 90(1):37–43
Schlenk D, Benson WH (2001) Target organ toxicity in marine and freshwater teleosts. Taylor and Francis, London
Schreck CB, Moyle PB (1990) Method of fish biology. American Fisheries Society, Bethesda, MD
Singh RK, Sharma B (1998) Carbufuran induced biochemical changes in Clarias batrachus. Pestic Sci 53:285–290
Stanic B, Andric N, Zoric S, Grubor-Lajsic G, Kovacevic R (2005) Assessing pollution in the Danube River near Novi Sad (Serbia) using several biomarkers in sterlet (Acipenser ruthenus L). Ecotoxicol Environ Saf 65(3):395–402. doi:10.1016/j.ecoenv.2005.08.005
Sun PL, Hawkins WE, Overstreet RM, Brown-Peterson NJ (2009) Morphological deformities as biomarkers in fish from contaminated rivers in Taiwan. Int J Environ Res Public Health 6:2307–2331. doi:10.3390/ijerph6082307
Svobodova Z, Dusek L, Hejtmanek M, Vykusova B, Smid R (1999) Bioaccumulation of mercury in various fish species from Orlik and Kamyk water reservoirs in the Czech Republic. Ecotoxicol Environ Saf 43(3):231–240. doi:10.1006/eesa.1999.1783
Tietz NW (1970) Fundamentals of clinical chemistry. Saunders Co, Philadelphia, PA 302
Tomlinson DL, Wilson JG, Harris CR, Jeffrey DW (1980) Problems in the assessment of heavy-metal levels in estuaries and the formation of a pollution index. Helgol Mar Res 33(1–4):566–575. doi:10.1007/BF02414780
Tuvikene A, Huuskonen S, Koponen K, Ritola O, Mauer U, Lindström-Seppä P (1999) Oil shale processing as a source of aquatic pollution: monitoring of the biologic effects in caged and feral freshwater fish. Environ Health Perspect 107(9):745–752
Van Dyk JC, Cochrane MJ, Wagenaar GM (2012) Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 87:301–311. doi:10.1016/j.chemosphere.2011.12.002
Varol M (2011) Assessment of heavy metal contamination in sediments of the Tigris River (Turkey) using pollution indices and multivariate statistical techniques. J Hazard Mat 195:355–364. doi:10.1016/j.jhazmat.2011.08.051
Varol M, Şen B (2012) Assessment of nutrient and heavy metal contamination in surface water and sediments of the upper Tigris River, Turkey. Catena 92:1–10. doi:10.1016/j.catena.2011.11.011
Vidal-Liñán L, Bellas J, Campillo JA, Beiras R (2010) Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain). Chemosphere 78(3):265–272. doi:10.1016/j.chemosphere.2009.10.060
Vieira LR, Gravato C, Soares AMVM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416–1427. doi:10.1016/j.chemosphere.2009.06.005
Wang C, Lu GH, Song WT, Xu S, Wang PF (2010) Integrated biomarker response index for the assessment of environmental stress of the Yangtze River (Nanjing section). Fish Physiol Biochem 36(4):1069–1078. doi:10.1007/s10695-010-9384-9
Wang JW, Liu RM, Zhang PP, Yu WW, Shen ZY, Feng CH (2014) Spatial variation, environmental assessment and source identification of heavy metals in sediments of the Yangtze River Estuary. Mar Pollut Bull 87:364–373. doi:10.1016/j.marpolbul.2014.07.048
Weatherley AH, Gill HS (1987) The biology of fish growth. Academic Press, London, pp 147–173
Westgard JO, Poquette MA (1972) Determination of serum albumin with the “SMA 12/60” by a Bromcresol green dye-binding method. Clin Chem 18:647–653
Yi Y, Yang Z, Zhang S (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159(10):2575–2585. doi:10.1016/j.envpol.2011.06.011
Yu RL, Yuan X, Zhao YH, Hu GR, Tu XL (2008) Heavy metal pollution in intertidal sediments from Quanzhou Bay, China. J Environ Sci 20:664–669. doi:10.1016/S1001-0742(08)62110-5
Zahra A, Hashmi MZ, Malik RN, Ahmed Z (2014) Enrichment and geo-accumulation of heavy metals and risk assessment of sediments of the Kurang Nallah-Feeding tributary of the Rawal Lake Reservoir, Pakistan. Sci Total Environ 470–471:925–933. doi:10.1016/j.scitotenv.2013.10.017
Zhang J, Fischer C (2006) A simplified resorcinol method for direct spectrophotometric determination of nitrate in seawater. Mar Chem 99:220–226. doi:10.1016/j.marchem.2005.09.008
Zhang H, Shan B (2008) Historical records of heavy metal accumulation in sediments and the relationship with agricultural intensification in the Yangtze-Huaihe region, China. Sci Total Environ 399:113–120. doi:10.1016/j.scitotenv.2008.03.036
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Omar, W.A., Saleh, Y.S. & Marie, MA.S. The use of biotic and abiotic components of Red Sea coastal areas as indicators of ecosystem health. Ecotoxicology 25, 253–266 (2016). https://doi.org/10.1007/s10646-015-1584-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-015-1584-8