Heavy Metals and Antibiotic Resistant Bacteria in Green Turtles are Indicators of Environmental Pollution
Freshly laid eggs from green turtles, Chelonia mydas,
were randomly collected from Ras Al-Hadd Reserve, Oman.
Eggshells taken from eggs and sand collected from the body chamber
were analyzed for eight heavy metals (Al, Br, Cd, Co, Cu, Fe, S, and
Zn) using inductively coupled plasma mass spectrometry (ICP).
Heavy metal concentrations varied significantly (P<0.05) between
nest sand and eggshells. Zn values were significantly higher than the
other heavy metals. A total of 60 heterotrophic bacteria belong to
eight genera were isolated from fresh egg contents (albumen and
yolk). Resistance of the isolates to Ak = amikacin, Ak = amikacin,
Amp= ampicillin, Gm= gentamycin, Cn = chloramphenicol, Min =
minocycline, N = Neomycin, S= streptomycin, Smx =
sulphamethoxazole, Tmp = trimethoprim, Tob = tobramycin was
tested. More than 40% of the isolates were multiple resistant to 2-10
antibiotics. Most of the resistant strains were also resistant to Zn. The
value of these findings may indicate that the origin of pollution is of
human contaminated effluents.
[1] SN Al-Bahry, IY Mahmoud, AE Elshafie, A Al-Harthy, S Al-Ghafri, I
Al-Amri and AY Alkindi. Bacterial flora and antibiotic resistance from
eggs of green turtles Chelonia mydas: an indication of polluted effluents.
Marine Poll Bull. 41, pp. 214-221. 2009a
[2] SN Al-Bahry, Mahmoud, S Al-Rawahi and J Paulson. Egg
contamination as an indicator of environmental health. In: Impact of Egg
Contamination on Environmental Health. Nova Science Publisher Inc.
New York. 2011a.
[3] SN Al-Bahry, MA Al-Zadjali, IY Mahmoud and AE Elshafie.
Biomonitoring marine habitats in reference to antibiotic resistant
bacteria and ampicillin resistance determinants from oviductal fluid of
the nesting green sea turtle, Chelonia mydas. Chemosphere. 87, pp.
1308-1315. 2012.
[4] SK Al-Musharafi. Analysis of heavy metal in eggshells of green turtles,
Chelonia mydas, by scanning electron microscopy and x-ray
microanalysis. In: Biotechnology and Conservation of Species from Arid
Regions. Nova Science Publisher, Inc. New York, USA. p.p. 138-144.
2014.
[5] SH Al-Rawahy, AY Al Kindi, A Elshafie, IY Mahmoud IY, S.N. Al-
Bahry, S.S. Al-Siyabi, M.H. Mansour and A.A. Al-Kiyumi,
Accumulation of metals in the egg yolk and liver of hatchling of green
turtles Chelonia mydas at Ras Al Hadd, Sultanate of Oman. ANSI: J.
Biol. Sci. 7, pp. 925-930. 2007.
[6] M Foti, C. Giacopello, T Bottari, V Fisichella, D Rinaldo and C
Mamminac. Antibiotic resistance of Gram negatives isolates from
loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea.
Mar. Pollut. Bull. 58, pp. 1363-1366. 2009.
[7] SN Al-Bahry, IY Mahmoud, KI Al-Belushi, AE Elshafie, A Al-Harthy
and CK Bakheit. Coastal sewage discharge and its impact on fish with
reference to antibiotic resistant enteric bacteria and enteric pathogens as
bio-indicators of pollution. Chemosphere. 77, p.p. 1534-1539. 2009c
[8] SN Al-Bahry, IY Mahmoud, JR Paulson and SK Al- Musharafi.
Antibiotic resistant bacteria in terrestrial and aquatic environments: A
review. IAJAA. 4, p.p. 1-11. 2015.
[9] SK, Al-Musharafi Mahmoud IY and Al-Bahry SN. 2013b.
Contamination of marine fish by heavy metals from coastal sewage
treated effluent runoff. The Third Asian Conference on Sustainability,
Energy and the Environment. Osaka, Japan. IAFOR. Pp. 100-107. 2013
[10] Shahidul, and M Tanaka, Impacts of pollution on coastal and marine
ecosystems including coastal and marine fisheries and approach for
management: a review and synthesis. Marine Poll Bull. 48, pp. 624-649,
2004.
[11] FX Han, A Banin, WL Kingery, GB Triplett, LX, SJ Zhou Zheng and
WX Ding. New approach to studies of heavy metal redistribution in soil.
Adv Env Res. 8, pp. 113- 120. 2003.
[12] J Kojadinovic, M Potier, CM Le, RP Cosson, and P Bustamante.
Bioaccumulation of trace elements in pelagic fish from the Western
Indian Ocean. Environ. Pollut. 146, pp. 548-566. 2007.
[13] SN Al-Bahry, IY Mahmoud, A. Al-Khaifi, AE Elshafie and A. Al-
Harthy. Viability of multiple antibiotic resistant bacteria in distribution
lines of treated sewage effluent used for irrigation. Water Sci Technol.
60, pp. 2939-2948. 2009b.
[14] S Kim and DS Aga. Potential ecological and human health impacts of
antibiotics and antibiotic-resistant bacteria from wastewater treatment
plants. J Toxicol Environ Health B Crit Rev. 10, pp.559-573. 2007.
[15] Kümmerer K. Antibiotics in the aquatic environment. A review. Part I.
Chemosphere 75, 417-434. 2009a.
[16] Kümmerer K. 2009b. Antibiotics in the aquatic environment. A review.
Part II. Chemosphere, 75, 435-441. 2009a.
[17] IY Mahmoud, SN Al-Bahry and SK Al-Musharafi. Fresh water habitat
pollution by treated sewage effluent in relation to multiple-antibioticresistant
bacteria. APCBEES Procedia. 5, pp. 363-367. 2013.
[18] OL Akinbowale, H Peng, P Grant and MD Barton. Antibiotic and heavy
metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Ag. 30,
pp. 177-182. 2007.
[19] L Bass, CA Liebert, MD Lee, AO Summers, DG White, SG Thayer and
JJ Maurer. Incidence and characterization of integrons, genetic elements
mediating multiple-drug resistance in avian Escherichia coli.
Antimicrob. Agents Chemother. 43, pp. 2925-2929. 1999.
[20] CS Hölzel, C Müller, KS Harms, S Mikolajewski, S Schäfer, K
Schwaiger and J Bauer. Heavy metals in liquid pig manure in light of
bacterial antimicrobial resistance. Environ Res. 11, pp. 21-27. 2012.
[21] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Environmental
contamination by industrial effluents and sludge relative to heavy
metals. GEP 2, pp. 14-18. 2014a.
[22] JW, Edwards, KS Edyvane, VA Boxall, M Hamann and KL Soole,
Metal levels in seston and marine fish flesh near industrial and
metropolitan centres in South Australia. Marine Poll Bull. 42, pp. 389-
396. 2001.
[23] J Burger and M Gochfeld, Cadmium and lead in common terns (Aves:
Sterna hirundo): relationship between levels in parents and eggs.
Environ. Monit. Assess. 16, pp. 253-258. 1991.
[24] LA Grabowski, JLJ Houpis, WI Woods, and KA Johson, Seasonal
bioavailability of sediemt-associated heavy metals along the Mississippi
river floodplain. Chemosphere, 25, pp. 643-651. 2001.
[25] CLSI, Clinical Laboratory Standard Institution, Performance Standards
for Antimicrobial Susceptibility Testing; 17th Informational
Supplement. CLSI M100-S17. CLSI, Wayne, PA. 2007.
[26] SN Al-Bahry, IY Mahmoud, SK Al-Musharafi, IS Al-Gharaibi, NK Al-
Harthy, HA Al-Zadjali, Microbial and chemical pollution of water-wells
relative to sewage effluents in Oman. IJSEE. 1, pp. 35-56. 2014a.
[27] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal
contamination from treated sewage effluents. 11th International
Conference on Modelling, Monitoring and Management of Water
Pollution. WIT Transactions on Ecology and The Environment, New
Forest. UK. Vol. 164, pp. 381-389. 2012.
[28] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal
pollution from treated sewage effluent. Procedia APCBEES. 5, 344-348.
2013a.
[29] SK, Al-Musharafi, IY, Mahmoud and SN Al-Bahry.. Environmental
hazards and pollution from liquid waste lagoons. IPCBEE 69, pp. 1-5.
2014b.
[30] CJ Henry, KF Beal, RB Bury and R Goggans. Organochloride
pesticieds, PCB, trace elements and metals in western pond turtle eggs
for Oregon. Northwest Sci., 77, 46-53. 2003.
[31] ER Harper, JA St Leger, JA Westberg, L Mazzaro, T Schmitt, TH
Reidarson, M Tucker, DH Cross and B Puschner. Tissue heavy metal
concentrations of stranded California sea lions (Zalophus californianus)
in Southern California. Environ. Pollut. 147, pp. 677-682. 2007.
[32] MM Storelli, G Barone, A Storelli and GO Marcotrigiano. Total and
subcellular distribution of trace elements (Cd, Cu and Zn) in the liver
and kidney of green turtles (Chelonia mydas) from the Mediterranean
Sea. Chemosphere. 70, p. 908-913. 2008.
[33] Berger, MW LeChevallier, DJ Reasoner. Control of biofilm growth in
drinking water distribution systems. United States Environmental
Protection Agency, Office of Research and Development, Washington
D.C. 1992.
[34] JA Tree, RM Adams and DN Less. Chlorination of indicator bacteria
and viruses in primary sewage effluent. J. Appl. Microbiol. 69, pp. 2038-
2043. 2003.
[35] R Shrivastava, RK Upreti, SR Jain, KN Prasad, PK Seth and UC
Chaturvedi. Suboptimal chlorine treatment of drinking water leads to
selection of multidrug-resistant Pseudomonas aeruginosa. Ecotoxicol
Environ Safety. 58, pp. 277-283. 2004.
[36] Omani Standards (OS) 52/1 for Wastewater reuse and discharge.
Ministry of Environment Decree No 52/1-standards for the minimization
of pollution to air, water and soil. Ministry of Environment. Muscat,
Oman. 1996.
[37] World Health Organization (WHO). A compendium of standards for
wastewater reuse in the Eastern Mediterranean Region. Regional Office
for the Eastern Mediterranean. Regional Centre for Environmental
Health Activities. 2005.
[1] SN Al-Bahry, IY Mahmoud, AE Elshafie, A Al-Harthy, S Al-Ghafri, I
Al-Amri and AY Alkindi. Bacterial flora and antibiotic resistance from
eggs of green turtles Chelonia mydas: an indication of polluted effluents.
Marine Poll Bull. 41, pp. 214-221. 2009a
[2] SN Al-Bahry, Mahmoud, S Al-Rawahi and J Paulson. Egg
contamination as an indicator of environmental health. In: Impact of Egg
Contamination on Environmental Health. Nova Science Publisher Inc.
New York. 2011a.
[3] SN Al-Bahry, MA Al-Zadjali, IY Mahmoud and AE Elshafie.
Biomonitoring marine habitats in reference to antibiotic resistant
bacteria and ampicillin resistance determinants from oviductal fluid of
the nesting green sea turtle, Chelonia mydas. Chemosphere. 87, pp.
1308-1315. 2012.
[4] SK Al-Musharafi. Analysis of heavy metal in eggshells of green turtles,
Chelonia mydas, by scanning electron microscopy and x-ray
microanalysis. In: Biotechnology and Conservation of Species from Arid
Regions. Nova Science Publisher, Inc. New York, USA. p.p. 138-144.
2014.
[5] SH Al-Rawahy, AY Al Kindi, A Elshafie, IY Mahmoud IY, S.N. Al-
Bahry, S.S. Al-Siyabi, M.H. Mansour and A.A. Al-Kiyumi,
Accumulation of metals in the egg yolk and liver of hatchling of green
turtles Chelonia mydas at Ras Al Hadd, Sultanate of Oman. ANSI: J.
Biol. Sci. 7, pp. 925-930. 2007.
[6] M Foti, C. Giacopello, T Bottari, V Fisichella, D Rinaldo and C
Mamminac. Antibiotic resistance of Gram negatives isolates from
loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea.
Mar. Pollut. Bull. 58, pp. 1363-1366. 2009.
[7] SN Al-Bahry, IY Mahmoud, KI Al-Belushi, AE Elshafie, A Al-Harthy
and CK Bakheit. Coastal sewage discharge and its impact on fish with
reference to antibiotic resistant enteric bacteria and enteric pathogens as
bio-indicators of pollution. Chemosphere. 77, p.p. 1534-1539. 2009c
[8] SN Al-Bahry, IY Mahmoud, JR Paulson and SK Al- Musharafi.
Antibiotic resistant bacteria in terrestrial and aquatic environments: A
review. IAJAA. 4, p.p. 1-11. 2015.
[9] SK, Al-Musharafi Mahmoud IY and Al-Bahry SN. 2013b.
Contamination of marine fish by heavy metals from coastal sewage
treated effluent runoff. The Third Asian Conference on Sustainability,
Energy and the Environment. Osaka, Japan. IAFOR. Pp. 100-107. 2013
[10] Shahidul, and M Tanaka, Impacts of pollution on coastal and marine
ecosystems including coastal and marine fisheries and approach for
management: a review and synthesis. Marine Poll Bull. 48, pp. 624-649,
2004.
[11] FX Han, A Banin, WL Kingery, GB Triplett, LX, SJ Zhou Zheng and
WX Ding. New approach to studies of heavy metal redistribution in soil.
Adv Env Res. 8, pp. 113- 120. 2003.
[12] J Kojadinovic, M Potier, CM Le, RP Cosson, and P Bustamante.
Bioaccumulation of trace elements in pelagic fish from the Western
Indian Ocean. Environ. Pollut. 146, pp. 548-566. 2007.
[13] SN Al-Bahry, IY Mahmoud, A. Al-Khaifi, AE Elshafie and A. Al-
Harthy. Viability of multiple antibiotic resistant bacteria in distribution
lines of treated sewage effluent used for irrigation. Water Sci Technol.
60, pp. 2939-2948. 2009b.
[14] S Kim and DS Aga. Potential ecological and human health impacts of
antibiotics and antibiotic-resistant bacteria from wastewater treatment
plants. J Toxicol Environ Health B Crit Rev. 10, pp.559-573. 2007.
[15] Kümmerer K. Antibiotics in the aquatic environment. A review. Part I.
Chemosphere 75, 417-434. 2009a.
[16] Kümmerer K. 2009b. Antibiotics in the aquatic environment. A review.
Part II. Chemosphere, 75, 435-441. 2009a.
[17] IY Mahmoud, SN Al-Bahry and SK Al-Musharafi. Fresh water habitat
pollution by treated sewage effluent in relation to multiple-antibioticresistant
bacteria. APCBEES Procedia. 5, pp. 363-367. 2013.
[18] OL Akinbowale, H Peng, P Grant and MD Barton. Antibiotic and heavy
metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Ag. 30,
pp. 177-182. 2007.
[19] L Bass, CA Liebert, MD Lee, AO Summers, DG White, SG Thayer and
JJ Maurer. Incidence and characterization of integrons, genetic elements
mediating multiple-drug resistance in avian Escherichia coli.
Antimicrob. Agents Chemother. 43, pp. 2925-2929. 1999.
[20] CS Hölzel, C Müller, KS Harms, S Mikolajewski, S Schäfer, K
Schwaiger and J Bauer. Heavy metals in liquid pig manure in light of
bacterial antimicrobial resistance. Environ Res. 11, pp. 21-27. 2012.
[21] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Environmental
contamination by industrial effluents and sludge relative to heavy
metals. GEP 2, pp. 14-18. 2014a.
[22] JW, Edwards, KS Edyvane, VA Boxall, M Hamann and KL Soole,
Metal levels in seston and marine fish flesh near industrial and
metropolitan centres in South Australia. Marine Poll Bull. 42, pp. 389-
396. 2001.
[23] J Burger and M Gochfeld, Cadmium and lead in common terns (Aves:
Sterna hirundo): relationship between levels in parents and eggs.
Environ. Monit. Assess. 16, pp. 253-258. 1991.
[24] LA Grabowski, JLJ Houpis, WI Woods, and KA Johson, Seasonal
bioavailability of sediemt-associated heavy metals along the Mississippi
river floodplain. Chemosphere, 25, pp. 643-651. 2001.
[25] CLSI, Clinical Laboratory Standard Institution, Performance Standards
for Antimicrobial Susceptibility Testing; 17th Informational
Supplement. CLSI M100-S17. CLSI, Wayne, PA. 2007.
[26] SN Al-Bahry, IY Mahmoud, SK Al-Musharafi, IS Al-Gharaibi, NK Al-
Harthy, HA Al-Zadjali, Microbial and chemical pollution of water-wells
relative to sewage effluents in Oman. IJSEE. 1, pp. 35-56. 2014a.
[27] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal
contamination from treated sewage effluents. 11th International
Conference on Modelling, Monitoring and Management of Water
Pollution. WIT Transactions on Ecology and The Environment, New
Forest. UK. Vol. 164, pp. 381-389. 2012.
[28] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal
pollution from treated sewage effluent. Procedia APCBEES. 5, 344-348.
2013a.
[29] SK, Al-Musharafi, IY, Mahmoud and SN Al-Bahry.. Environmental
hazards and pollution from liquid waste lagoons. IPCBEE 69, pp. 1-5.
2014b.
[30] CJ Henry, KF Beal, RB Bury and R Goggans. Organochloride
pesticieds, PCB, trace elements and metals in western pond turtle eggs
for Oregon. Northwest Sci., 77, 46-53. 2003.
[31] ER Harper, JA St Leger, JA Westberg, L Mazzaro, T Schmitt, TH
Reidarson, M Tucker, DH Cross and B Puschner. Tissue heavy metal
concentrations of stranded California sea lions (Zalophus californianus)
in Southern California. Environ. Pollut. 147, pp. 677-682. 2007.
[32] MM Storelli, G Barone, A Storelli and GO Marcotrigiano. Total and
subcellular distribution of trace elements (Cd, Cu and Zn) in the liver
and kidney of green turtles (Chelonia mydas) from the Mediterranean
Sea. Chemosphere. 70, p. 908-913. 2008.
[33] Berger, MW LeChevallier, DJ Reasoner. Control of biofilm growth in
drinking water distribution systems. United States Environmental
Protection Agency, Office of Research and Development, Washington
D.C. 1992.
[34] JA Tree, RM Adams and DN Less. Chlorination of indicator bacteria
and viruses in primary sewage effluent. J. Appl. Microbiol. 69, pp. 2038-
2043. 2003.
[35] R Shrivastava, RK Upreti, SR Jain, KN Prasad, PK Seth and UC
Chaturvedi. Suboptimal chlorine treatment of drinking water leads to
selection of multidrug-resistant Pseudomonas aeruginosa. Ecotoxicol
Environ Safety. 58, pp. 277-283. 2004.
[36] Omani Standards (OS) 52/1 for Wastewater reuse and discharge.
Ministry of Environment Decree No 52/1-standards for the minimization
of pollution to air, water and soil. Ministry of Environment. Muscat,
Oman. 1996.
[37] World Health Organization (WHO). A compendium of standards for
wastewater reuse in the Eastern Mediterranean Region. Regional Office
for the Eastern Mediterranean. Regional Centre for Environmental
Health Activities. 2005.
@article{"International Journal of Biological, Life and Agricultural Sciences:69694", author = "S. K. Al-Musharafi and I. Y. Mahmoud and S. N. Al-Bahry", title = "Heavy Metals and Antibiotic Resistant Bacteria in Green Turtles are Indicators of Environmental Pollution", abstract = "Freshly laid eggs from green turtles, Chelonia mydas,
were randomly collected from Ras Al-Hadd Reserve, Oman.
Eggshells taken from eggs and sand collected from the body chamber
were analyzed for eight heavy metals (Al, Br, Cd, Co, Cu, Fe, S, and
Zn) using inductively coupled plasma mass spectrometry (ICP).
Heavy metal concentrations varied significantly (P", keywords = "Antibiotic resistance, bacteria, environment, heavy
metals, sea turtles.", volume = "9", number = "4", pages = "409-4", }
