Abstract
This work aimed at using Little Egrets (Egretta garzetta), for the first time in Egypt, as a bioindicator of heavy metal contamination from three different Egyptian land use types (Qillin within Kafr El-Sheikh (S1, agricultural), Toukh within Qalyubia (S2, semi-rural area), and Abu Rawash within Giza (S3, urban)). Concentrations of aluminum (Al), barium (Ba), cobalt (Co), cadmium (Cd), chromium (Cr), copper (Cu), manganese (Mn), iron (Fe), nickel (Ni), lead (Pb), and zinc (Zn) were analyzed in liver and kidney samples of twenty-six adult Little Egrets collected from the three localities during winter 2018. Moreover, the study calculated the Metal Pollution Index (MPI) to highlight the health of the surrounding environment using birds’ internal organs as a mirror. Results revealed that, throughout the three sampling sites, the total metal concentrations in liver samples exceeded that of the kidney, indicating that the liver is the target organ of metal accumulation. The Little Egret’s liver was found to be the best-recommended organ to use in future biomonitoring of Cu, Zn, Fe, Mn, and Ni, whereas Al, Co, Cr, Ba, Pb, and Cd can be monitored in the kidney. Cu and Pb were higher in the Little Egret’s tissues collected from the agricultural site (S1), whereas Ba, Ni, and Fe were higher in the semi-rural site (S2), followed finally by Cd in the urbanized site (S3). The concentrations of trace elements reported in Little Egrets were within the known background level for water birds. However, alarming concentrations were found for Ni levels in liver (from Qillin and Toukh), as well as Pb and Cr levels in kidney samples (from the three localities). MPI of the eleven studied metals in both liver and kidney of the studied species decreased in the order Qillin (24.36) > Abu Rawash (17.98) > Toukh (3.90). In the three investigated localities, the overall calculated MPI values were higher than one, indicating that the ecosystem is polluted. The study suggested using Little Egrets as a bioindicator of metal contamination.
Similar content being viewed by others
References
Abdiem OO (2011) An assessment of soil heavy metal pollution by various allied artisans in automobile workshop in Osun state, Nigeria. Elec J Env Agricult Food Chem Title 10:1881–1886
Al Naggar YA, Naiem EA, Seif AI, Mona MH (2013) Honey bees and their products as a bio-indicator of environmental pollution with heavy metals. Mellifera 13:10–20
Boncompagni E, Muhammad A, Jabeen R, Orvini E, Gandini C, Sanpera C, Ruiz X, Fasola M (2003) Egrets as monitors of trace-metal contamination in wetlands of Pakistan. Arch Environ Contam Toxicol 45(3):399–406. https://doi.org/10.1007/s00244-003-0198-y
Burger J, Gochfeld M (2004) Metal levels in eggs of common terns (Sterna hirundo) in New Jersey: temporal trends from 1971 to 2002. Environ Res 94:336–343
Capdevielle MC, Hart LE, Goff J, Scanes CG (1998) Aluminum and acid effects on calcium and phosphorus metabolism in young growing chickens (Gallus gallus domesticus) and mallard ducks (Anas platyrhynchos). Arch Environ Contam Toxicol 35:82–88
Carson BL, Ellis HV, McCann JL (1986) Toxicology and biological monitoring of metals in humans. Lewis publishers, Inc., Chelsea, pp 128–135
Clark AJ, Scheuhammer AM (2003) Lead poisoning in up-land foraging birds of prey in Canada. Ecotoxicology 12:23–30
Degernes LA (2008) Waterfowl toxicology: a review. Vet Clin N Am Exot Anim Pract 11:283–300
ESA (2007) Egyptian General Survey Authority, Ministry of State for Local Development. http://www.eip.gov.eg/Periodicals/WasfMisr/2008/kaf.pdf
Fakayode S, Onianwa P (2002) Heavy metal contamination of soil and bioaccumulation in Guinea grass (Panicum maximum) around Ikeja industrial estate, Lagos, Nigeria. Environ Geol 43:145–150
Ferreira AP (2010) Estimation of heavy metals in little blue heron (Egretta caerulea) collected from Sepetiba bay, Rio de Janeiro, Brazil. Braz J Oceanogr 58(4):269–274
Goutner V, Becker PH, Liordos V (2011) Organochlorines and mercury in livers of great cormorants (Phalacrocorax carbo sinensis) wintering in northeastern Mediterranean wetlands in relation to area, bird age, and gender. Sci Total Environ 409(4):710–718
Horai S, Watanabe I, Takada H, Iwamizu Y, Hayashi T, Tanabe S, Kuno K (2007) Trace element accumulations in 13 avian species collected from the Kanto area, Japan. Sci Total Environ 373:512–525
Jiang X, Lu WX, Zhao HQ, Yang QC, Yang ZP (2014) Potential ecological risk assessment and prediction of soil heavy-metal pollution around coal gangue dump. Nat Hazards Earth Syst Sci 14:1599–1610
Johansen P, Mulvad G, Pedersen HS, Hansen JC, Riget F (2006) Accumulation of cadmium in livers and kidneys in Greenlanders. Sci Total Environ 372(1):58–63
Jovi M, Stankovi S (2014) Determination of marine pollution by comparative analysis of metal pollution indices. Arch Biol Sci Belgrade 66(3):1205–1215
Jovi M, Stankovi A, Slavkovi-Beskoski L, Tomi I, Degetto S, Stankovi S (2011) Mussels as a bioindicator of the environmental quality of the coastal water of the Boka Kotorska Bay (Montenegro). J Serbian Chem Soc 76:933–946
Kendrick M, Moy M, Plishka M, Robinson K (1992) Metals in biological systems. Ellis Horwood, England, p 183
Kim J, Oh J-M (2013) Assessment of trace metals in four bird species from Korea. Environ Monit Assess 185:6847–6854
Kim J, Oh J-M (2015) Tissue distribution of heavy metals in heron and egret chicks from Pyeongtaek, Korea. Arch Environ Contam Toxicol 68:283–291
Kim J, Oh J-M (2016) Assessment of trace element concentrations in birds of prey in Korea. Arch Environ Contam Toxicol 71(1):26–34
Kitowski I, Wiacek D, Sujak A, Komosa A, Swietlicki M (2017) Factors affecting trace element accumulation in livers of avian species from East Poland. Turk J Zool. https://doi.org/10.3906/zoo-1606-43
Korbecki J, Gutowska I, Chlubek D, Baranowska-Bosiacka I (2019) Lead (Pb) in the tissues of Anatidae, Ardeidae, Sternidae and Laridae of the northern hemisphere: a review of environmental studies. Environ Sci Pollut Res 26:12631–12647
Lafabrie C, Pergent-Martini C, Pergent G (2008) Metal contamination of Posidonia oceanica meadows along the Corsican coastline (Mediterranean). Environ Pollut 151:262–268
Leary S (ed.) (2013) AVMA Guidelines for the Euthanasia of Animals. 2013 edn. American Veterinary Medical Association, Schaumburg, pp 102
Lucia M, André J, Gontier K, Diot N, Veiga J, Davail S (2010) Trace element concentrations (mercury, cadmium, copper, zinc, Lead, aluminum, nickel, arsenic and selenium) in some aquatic birds of the Southwest Atlantic coast of France. Arch Environ Contam Toxicol 58:844–853
Malik RN, Zeb N (2009) Assessment of environmental contamination using feathers of Bubulcus ibis L., as a biomonitor of heavy metal pollution, Pakistan. Ecotoxicology 18:522–536
Mansour SA, Soliman SS, Soliman KM (2016) Monitoring of heavy metals in the environment using bats as bioindicators: first study in Egypt. Vespertilio 18:61–78
Mateo R, Taggart M, Meharg AA (2003) Lead and arsenic in bones of birds of prey from Spain. Environ Pollut 126:107–114
Maurya PK, Malik DS (2018) Bioaccumulation of heavy metals in tissues of selected fish species from ganga river, India, and risk assessment for human health, Human and Ecological Risk Assessment: An International Journal
Mmolawa KB, Likuky AS, Gaboutloeloe GK (2011) Assessment of heavy metal pollution in soils along major roadside areas in Botswana. Afr J Environ Sci Technol 5:186–196
Nam DH, Lee DP (2009) Abnormal lead exposure in globally threatened cinereous vultures (Aegypius monachus) wintering in South Korea. Ecotoxicology 18:225–229
Nardiello V, Fidalgo LE, López-Beceiro A, Bertero A, Martínez-Morcillo S, Míguez MP, Soler F, Caloni F, Pérez-López M (2019) Metal content in the liver, kidney, and feathers of northern gannets, Morus bassanus, sampled on the Spanish coast. Environ Sci Pollut Res Int 26(19):19646–19654
Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) (2011) Handbook on the toxicology of metals. Academic press, Amsterdam, Boston
Norwood WP, Borgmann U, Dixon DG (2007) Interactive effects of metals in mixtures on bioaccumulation in the amphipod Hyalella azteca. Aquat Toxicol 84(2):255–267
Ombugadu A, Mwansat GS, Manu SA, Chaskda AA, Ottosson U, Njila LH, Karau SD (2014) Comparison on bioaccumulation of heavy metals in birds and plant species in Amurum forest reserve and the Nigerian National Petroleum Corporation (NNPC) refinery area of Kaduna, Nigeria. Int J Adv Stud Eng Sci Invent 2(1):26–32
Orłowski G, Kaminski P, Kasprzykowski Z, Zawada Z, Koim-Puchowska B, Szady-Grad M, Klawe JJ (2012) Essential and nonessential elements in nestling rooks Corvus frugilegus from eastern Poland with a special emphasis on their high cadmium contamination. Arch Environ Contam Toxicol 63:601–611
Outridge PM, Scheuhammer AM (1993a) Bioaccumulation and toxicology of chromium: implications for wildlife. Rev Environ Contam Toxicol 130:31–77
Outridge PM, Scheuhammer AM (1993b) Bioaccumulation and toxicology of nickel: implications for wild mammals and birds. Environ Rev 1:172–197. https://doi.org/10.1139/a93-013
Rita CAS, Mitiko SEGM, Paulo TMSO (2018) The great egret (Ardea alba) as a bioindicator of trace element contamination in the Sao Paulo Metropolitan Region, Brazil. J Radioanal Nucl Chem 315:447–458
Rothschild RFN, Duffy LK (2005) Mercury concentrations in muscle, brain and bone of Western Alaskan waterfowl. Sci Total Environ 349(1–3):277–283
Salah-Eldein AM, Gamal-Eldein MA, Lamiaa IM (2012) Resident wild birds as bio-indicator for some heavy metals pollution in Lake Manzala. Suez Canal Vet Med J 17(1):109–121
Scheuhammer AM (1987) The chronic toxicity aluminum, cadmium, mercury and lead in birds: a review. Environ Pollut 46:263–295
Silva RCA, Saiki M, Moreira EG, Oliveira PTMS (2018) The great egret (Ardea alba) as a bioindicator of trace element contamination in the Sao Paulo metropolitan region, Brazil. J Radioanal Nucl Chem 315:447–458
Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharm 43(3):246–253. https://doi.org/10.4103/0253-7613.81505
Skerfving S, Bergdahl IA (2007) Lead. In: Nordberg GF, Fowler BA, Nordberg M, Friberg LT (eds) Handbook on the toxicology of metals, 3rd edn. Elsevier Science Publishers B.V, Amsterdam, pp 599–643
Taggart MA, Green AJ, Mateo R, Svanberg F, Hillstrom L, Meharg AA (2009) Metal levels in the bones and livers of globally threatened marbled teal and white-headed duck from El Hondo, Spain. Ecotoxicol Environ Saf 72:1–9. https://doi.org/10.1016/j.ecoenv.2008.07.015
Teodorovic I, Djukic N, Maletin S, Miljanovic B, Jugovac N (2000) Metal pollution index: proposal for freshwater monitoring based on trace metal accumulation in fish. Tiscia 32:55–60
Thirulogachandar AME, Rajeswari M, Ramya S (2014) Assessment of heavy metals in Gallus and their impacts on human. Int J Sci Res Publ 4(6):1–8
US Environmental Protection Agency (1987) Drinking water criteria document for copper. Environmental Criteria and Assessment Office, Cincinnati, OH, for the office of Drinking water, Washington, DC. ECAO-CIN-417
Usero J, Gonzalez-Regalado E, Gracia I (1997) Trace metal in the bivalve mollusks Ruditapes decussates and Ruditapes philippinarum from the Atlantic coast of southern Spain. Environ Int 23:291–298
Usero J, Morillo J, Gracia I (2005) Heavy metal concentrations in mollusks from the Atlantic coast of southern Spain. Chemosphere 59:1175–1181
US-Government (2001) Control of emissions of hazardous air pollutants from mobile sources: final rule. Fed Regist 66:80–86
Vizuete J, Pérez-Lopez M, Miguez-Santiyan MP, Hernandez-Moreno D (2018) Mercury (hg), Lead (Pb), cadmium (cd), selenium (se), and arsenic (as) in liver, kidney, and feathers of gulls. Part of the reviews of environmental contamination and toxicology Book series: A Review. pp 1–62
Yasmeen R, Muhammad HA, Bokhari SS, Rafi U, Shakoor A, Qurashi AW (2019) Assessment of heavy metals in different organs of cattle egrets (Bubulcus ibis) from a rural and urban environment in Pakistan. Environ Sci Pollut Res 26:13095–13102
Zarrintab M, Mirzaei R (2017) Evaluation of some factors influencing on variability in bioaccumulation of heavy metals in rodents species: Rombomys opimus and Rattus norvegicus from Central Iran. Chemosphere 169:194–203
Zarrintab M, Mirzaei R (2018) Tissue distribution and oral exposure risk assessment of heavy metals in an urban bird: magpie from Central Iran. Environ Sci Pollut Res 25:17118–17127
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Soliman, K.M., Mohallal, E.M.E. & Alqahtani, A.R.M. Little egret (Egretta garzetta) as a bioindicator of heavy metal contamination from three different localities in Egypt. Environ Sci Pollut Res 27, 23015–23025 (2020). https://doi.org/10.1007/s11356-020-08736-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-08736-x