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Trace elements in feathers and eggshells of two tropical seabirds from Malaysia



1Faculty of Science and Marine Environment, Universiti Malaysia Terengganu (UMT), 21300 Kuala Nerus, Malaysia
2Current address: Nature Conservation Department, Ministry of Environment, PO Box 13793, Tripoli, Libya
3Institute of Oceanography and Environment (INOS), Universiti Malaysia Terengganu (UMT), 21300 Kuala Nerus, Malaysia *(miman@umt.edu.my)

Received 18 February 2021; Accepted 06 July 2021

Date Published: 2021/10/15
Date Online: 2021/10/14

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HAMZA, A., HISHAM, A.S., SURATMAN, S., BIDAI, J.A. & SHAZILI, N.A.M. 2021. Trace elements in feathers and eggshells of two tropical seabirds from Malaysia. Marine Ornithology 49: 335-341.

Key words: trace metals, seabird feathers, bioaccumulation, South China Sea


Seabird feathers and eggshells are used as bio-monitors for trace metal contamination. Eleven trace element concentrations in wing primaries (n = 21) and eggshells (n = 8) are reported herein for two resident seabirds, Bridled Tern Onychoprion anaethetus and Black-naped Tern Sterna sumatrana, at Pulau Ling and Pulau Tokung Burung, Malaysia. Metal concentration followed the pattern Zn > Cr > Mn > Sr > Cu > Se > Ba > Pb > Cd > Ga > Li. Significant positive correlations existed among all trace metals, except for Cr in Black-naped Tern and Li and Cd in Bridled Tern feathers. We also analyzed metal concentrations in eggshells, and for Bridled Tern, the concentration pattern was Zn > Mn > Se > Sr > Ba > Pb > Co > Cu > Cd, whereas for Black-naped Tern it was Cr > Zn > Mn > Ba > Sr > Se > Cu> Co > Pb. A pairwise positive correlation was significant among most trace metals in feather samples, indicating synergistic effects of two or more elements. More studies are needed to build a baseline database of trace metal concentrations in seabirds of Southeast Asia, as little research on this subject has been conducted in this region.


ABBASI, N.A., KHAN, M.U., JASPERS, V.L., CHAUDHRY, M.J. & MALIK, R.N. 2015. Spatial and interspecific variation of accumulated trace metals between remote and urbane dwelling birds of Pakistan. Ecotoxicology and Environmental Safety 113: 279-286. doi:10.1016/j.ecoenv.2014.11.034

ADRIANO, D.C. 2001. Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability, and Risks of Metal, 2nd Edition. New York, USA: Springer. doi:10.1007/978-0-387-21510-5

ANTONINA, A.N., SHAZILI, N.A.M., KAMARUZZAMAN, B.Y., ONG, M.C., ROSNAN, Y. & SHARIFAH, F.N. 2013. Geochemistry of the rare earth elements distribution in Terengganu coastal waters: A study case from Redang Island marine sediment. Open Journal of Marine Science 3: 154-159. doi:10.4236/ojms.2013.33017

ARIFFIN, M.M., ADIANA, G., BIDAI, J., HING, L.S., NURULNADIA, M.Y., ONG, M.C., SHAARI, H. & PRADIT, S. 2019. Data on dissolved metals in Terengganu waters of South China Sea during pre-, post-, and Northeast Monsoon season. Data Brief 27: 104806. doi:10.1016/j.dib.2019.104806

BORGHESI, F., MIGANI, F., ANDREOTTI, A., BACCETTI, N., BIANCHI, N., BIRKE, M. & DINELLI, E. 2016. Metals and trace elements in feathers: A geochemical approach to avoid misinterpretation of analytical responses. Science of The Total Environment 544: 476-494. doi:10.1016/j.scitotenv.2015.11.115

BURGER, J. 1994. Heavy metals in avian eggshells: another excretion method. Journal of Toxicology and Environmental Health 41: 207-220. doi:10.1080/15287399409531837

BURGER, J. 1993. Metals in avian feathers: bioindicators of environmental pollution. Reviews in Environmental Toxicology 5: 203-311.

BURGER, J. & GOCHFELD, M. 1991. Lead, mercury, and cadmium in feathers of tropical terns in Puerto Rico and Australia. Archives of Environmental Contamination and Toxicology 21: 311-315. doi:10.1007/BF01055351

BURGER, J. & GOCHFELD, M. 2000. Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Science of the Total Environment 257: 37-52. doi:10.1016/s0048-9697(00)00496-4

BURGER, J., SCHREIBER, E.A.E. & GOCHFELD, M. 1992. Lead, cadmium, selenium and mercury in seabird feathers from the tropical mid‐pacific. Environmental Toxicology and Chemistry 11: 815-822. doi:10.1002/etc.5620110610

CHOW T.J. & SNYDER, C.B. 1980. Barium in marine environments: A potential indicator of drilling contamination. Proceedings on Research on Environmental Fate and Effects of Drilling Fluids and Cuttings Symposia 1980: 723-736.

DABWAN, A.H. & TAUFIQ, M. 2016. Bivalves as bio-indicators for heavy metals detection in Kuala Kemaman, Terengganu, Malaysia. Indian journal of science and Technology 99: 1-6. doi:10.17485/ijst/2016/v9i9/88708

DE ASSIS PADILHA, J., DA CUNHA, L.S.T., DE CASTRO, R.M., MALM, O. & DORNELES, P.R. 2018. Exposure of Magnificent Frigatebird Fregata magnificens and Brown Booby Sula leucogaster to metals and selenium in Rio de Janeiro State (Brazil) coastal waters. Orbital: The Electronic Journal of Chemistry 10: 254-261. doi:10.17807/orbital.v10i2.1050

DOLCI, N.N., SÁ, F., DA COSTA MACHADO, E., KRUL, R. & NETO, R.R. 2017. Trace elements in feathers and eggshells of brown booby Sula leucogaster in the Marine National Park of Currais Islands, Brazil. Environmental Monitoring and Assessment 189: 496. doi:10.1007/s10661-017-6190-1

ESPÍN, S., GARCÍA-FERNÁNDEZ, A.J., HERZKE, D. ET AL. 2014. Sampling and contaminant monitoring protocol for raptors. Research Networking Programme—Research and Monitoring For and With Raptors in Europe (EURAPMON). Strasbourg, France: European Science Foundation. [Accessed at http://www.eurapmon.net/sites/default/files/pdf-s/summary_sampling_and_contaminant_monitoring_protocol_for_raptors_eurapmon_2ndmay_final.pdf on 25 March 2021].

FUAD, M.M., SHAZILI, N.A.M. & FARIDAH, M. 2013. Trace metals and rare earth elements in Rock Oyster Saccostrea cucullata along the east coast of Peninsular Malaysia. Aquatic Ecosystem Health & Management 16: 78-87. doi:10.1080/14634988.2013.762327

FURNESS, R.W. 1993. Birds as Monitors of Pollutants. In: FURNESS, R.W. (Ed.) Birds As Monitors Of Environmental Change. Dordrecht, Netherlands: Springer. doi:10.1007/978-94-015-1322-7_3.

GARCÍA-FERNÁNDEZ, A.J., ESPÍN, S. & MARTÍNEZ-LÓPEZ, E. 2013. Feathers as a biomonitoring tool of polyhalogenated compounds: a review. Environmental Science & Technology 47: 3028-3043. doi:10.1021/es302758x

HAMZA, A. & HO, W.C. 2020. Updates on seabirds of the northern Seribuat Islands, Pahang, Malaysia. Marine Ornithology 48: 1-7.

HAMZA, A., WONG, C. & AHMAD, A. 2016. Pulau Ling: an important seabird hotspot on the east coast of Peninsular Malaysia. Journal of Asia-Pacific Biodiversity 9: 437-442. doi:10.1016/j.japb.2016.04.006

HASHMI, M.Z., MALIK, R.N. & SHAHBAZ, M. 2013. Heavy metals in eggshells of cattle egret Bubulcus ibis and little egret Egretta garzetta from the Punjab province, Pakistan. Ecotoxicology and Environmental Safety 89: 158-165. doi:10.1016/j.ecoenv.2012.11.029

HEINZ, G.H. 1996. Selenium In Birds. In: BEYER, W. N., HEINZ, G. H. & REDMON-NORWOOD, A.W (Eds.) Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. Boca Ration, USA: CRC/Lewis Publishers.

HUSSEIN, M., YONEDA, K., MOHD-ZAKI, Z., AMIR, A. & OTHMAN, N. (2021). Heavy metals in leachate, impacted soils and natural soils of different landfills in Malaysia: An alarming threat. Chemosphere 267: 128874. doi:10.1016/j.chemosphere.2020.128874

KAMARUZZAMAN, B.Y., ONG, M.C., JALAL, K.C.A., SHAHBUDIN, S. & NOR, O.M. 2009. Accumulation of lead and copper in Rhizophora apiculata from Setiu mangrove forest, Terengganu, Malaysia. Journal of Environmental Biology 30: 821-824.

KHADEMI, N., RIYAHI-BAKHTIARI, A., SOBHANARDAKANI, S., REZAIE-ATAGHOLIPOUR, M. & BURGER, J. 2015. Developing a bioindicator in the Northwestern Persian Gulf, Iran: trace elements in bird eggs and in coastal sediments. Archives of Environmental Contamination and Toxicology 68: 274-282. doi:10.1007/s00244-014-0084-9

LAM, J.C., TANABE, S., LAM, M.H., & LAM, P.K. 2005. Risk to breeding success of waterbirds by contaminants in Hong Kong: evidence from trace elements in eggs. Environmental pollution 135: 481-490. doi:10.1016/j.envpol.2004.11.021

MANJULA, M., MOHANRAJ, R., & DEVI, M.P. 2015. Biomonitoring of heavy metals in feathers of eleven common bird species in urban and rural environments of Tiruchirappalli, India. Environmental Monitoring and Assessment 187: 187-267. doi:10.1007/s10661-015-4502-x

MNS Bird Conservation Council. 2015. A Checklist of the Birds of Malaysia, 2nd Edition. Kuala Lumpur, Malaysia: Malaysian Nature Society, Bird Conservation Council, Malaysia.

MORA, M.A., TAYLOR, R.J. & BRATTIN, B.L. 2007. Potential ecotoxicological significance of elevated concentrations of strontium in eggshells of passerine birds. The Condor 1: 199-205. doi:10.1093/condor/109.1.199

MOURA, J.F., TAVARES, D.C., LEMOS, L.S., SILVEIRA, V.V.B., SICILIANO, S, & HAUSER-DAVIS, R.A. 2018. Variation in mercury concentration in juvenile Magellanic penguins during their migration path along the Southwest Atlantic Ocean. Environmental Pollution 238: 397-403. doi:10.1016/j.envpol.2018.03.021

MUÇOZ CIFUENTES, J., BECKER, P.H., SOMMER, U., PACHECO, P. & SCHLATTER, R. 2003. Seabird eggs as bioindicators of chemical contamination in Chile. Environmental Pollution 126: 123-137. doi:10.1016/S0269-749102.00400-1

OHLENDORF, H.M. & HEINZ, G.H. 2011. Selenium in birds. In: BEYER, W.N. & MEADOR, J.P. (Eds.) Environmental Contaminants in Biota: Interpreting Tissue Concentrations, 2nd Edition. Boca Raton, USA: CRC Press. [Accessed at https://core.ac.uk/download/pdf/188109049.pdf on 10 December 10 2020.]

PERRY JR, H.M., KOPP, S.J., PERRY, E F. & ERLANGER, M.W. 1989. Hypertension and associated cardiovascular abnormalities induced by chronic barium feeding. Journal of Toxicology and Environmental Health 28: 373-388. doi:10.1080/15287398909531356

POONG, J.H., TEE, L.S., TAN, E. ET AL. 2020. Level of heavy metals in bamboo sharks Chiloscyllium sp. in straits of Malacca, Malaysia. Malaysian Journal of Analytical Sciences 24: 546-557.

RAHOUMA, M., SHUHAIMI-OTHMAN, M. & COB, Z.C. 2013. Assessment of selected heavy metals Zn, Mn, Pb, Cd, Cr and Cu. in different species of Acetes shrimp from Malacca, Johor and Terengganu, Peninsular Malaysia. Journal of Environmental Science and Technology 6: 50-56. doi:10.3923/jest.2013.50.56

RASOOLI, R., SALAMATIAN, I., AGHAZAMANI, M., ORYAN, A., SALEHI, M. & ROHOLLAHZADEH, H. 2018. Effect of lithium toxicity in roiler. Journal of World Poultry Research 8: 59-65.

SEBASTIANO, M., BUSTAMANTE, P., COSTANTINI, D. ET AL. 2016. High levels of mercury and low levels of persistent organic pollutants in a tropical seabird in French Guiana, the Magnificent Frigatebird, Fregata magnificens. Environmental Pollution 214: 384-393. doi:10.1016/j.envpol.2016.03.070

SHAZILI, N.A.M., KAMARUZZAMAN, B.Y., ANTONINA, N.A. ET AL. 2007. Interpretation of anthropogenic input of metals in the South China Sea bottom sediments off Terengganu Malaysia coastline using AI as a reference element. Aquatic Ecosystem Health & Management 10: 47-56. doi:10.1080/14634980701201681

SUN, T., WU, H., WANG, X., JI, C., SHAN, X. & LI, F. 2019. Evaluation on the biomagnification or biodilution of trace metals in global marine food webs by meta-analysis. Environmental Pollution 264: 113856. doi:10.1016/j.envpol.2019.113856

TKA, T.N.A., NURULNADIA, M.Y., ZALEHA, K. ET AL. 2019. Accumulation of heavy metals in farmed lates calcarifer of a tropical coastal lagoon. Oriental Journal of Chemistry 35: 1187-1194.

VAN ASWEGEN, J.D., NEL, L., STRYDOM, N.A., MINNAAR, K., KYLIN, H. & BOUWMAN, H. 2019. Comparing the metallic elemental compositions of Kelp Gull Larus dominicanus eggs and eggshells from the Swartkops Estuary, Port Elizabeth, South Africa. Chemosphere 221: 533-542. doi:10.1016/j.chemosphere.2019.01.013

XU, L.Q., LIU, X.D., SUN, L.G. ET AL. 2011. A 700-year record of mercury in avian eggshells of Guangjin Island, South China Sea. Environmental Pollution 159: 889-896. doi:10.1016/j.envpol.2010.12.021

XU, L.Q., WU, L.B., ZHANG, Y.H. & ZHAO, J.J. 2019. Transport of cobalt and silver from the ocean to a reef island by seabirds in the South China Sea. Journal of Geophysical Research: Biogeosciences 124: 3005-3014. doi:10.1029/2019JG005264

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