Abstract
The excessive enrichment of trace elements, such as Pb and Cd, from food may contribute to the decline of migratory red-crowned cranes (Grus japonensis) in China. To test this prediction, we determined the concentrations of Pb and Cd, as well as further macro and trace elements (Ca, Mg, Cu, Zn) in the target species and their prey (sediment, reed root, mollusk, arthropods, and common fish species) in both the wintering (Yancheng wetland) and breeding sites (Zhalong wetland) of cranes in China. The maximum concentrations of Pb (130 mg kg−1 dry weight (dw)) and Cd (10.60 mg kg−1 dw) in the sediments of breeding site and the maximum concentration of Cd (4.50 mg kg−1 dw) in the sediments of wintering site exceeded the probable effect level values (91.30 mg kg−1 for Pb and 3.53 mg kg−1for Cd), suggesting the potential exposure risk of the examined species. Indeed, Pb and Cd contents of essential foods, i.e., aquatic animals, sampled in two sites were above the limit of allowable concentration recommended by the Joint Food and Agriculture Organization of the United Nations/World Health Organization food standards program. Approximately 80, 31.4, and 60.3 mg kg−1 dw of Pb were detected in the eggshells, liver, and kidney, respectively, of the target species, and the values are above the levels of concern (1.7 mg kg−1 for eggshell and 30 mg kg−1 for liver and kidney) in common birds. Nevertheless, the increased Pb and Cd levels in the prey and bodies of the red-crowned cranes did not induce the levels of Ca and Mg depletion. Average contents of the macronutrients, Ca (1.38 g kg−1 dw) and Mg (1.32 g kg−1 dw), in the liver of the examined species exceeded the background concentrations (0.2–0.4 g kg−1 for Ca and 0.4–0.8 g kg−1 for Mg) in the liver of birds. Consumption of Ca-rich foods, e.g., grits and exoskeleton species, may aid in compensating the possible loss caused by the increased Pb and Cd concentrations in the bodies of the cranes.
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References
Ackerman JT, Herzog MP, Schwarzbach SE (2013) Methylmercury is the predominant form of mercury in bird eggs. Environ Sci Technol 47:2052–2060
Bird Life International (2017) Grus japonensis: IUCN 2017. IUCN red list of threatened species. http://www.birdlife.org/ (on 9 March, 2017)
Burger J (1994) Heavy metals in avian eggshells: another excretion method. J Toxic Environ Health 41:207–220
Burger J, Gochfeld M (1993) Lead and cadmium accumulation in eggs and edgling seabirds in the New York Bight. EnvironToxicol Chem 12:261–267
Burger J, Gochfeld M, Jeitner C, Snigaroff D, Snigaroff D, Stamm T, Volz C (2008) Assessment of metals in down feathers of female common eiders and their eggs from Aleutians: arsenic, cadmium, chromium, lead, manganese, mercury, and selenium. Environ Monit Assess 143(1–3):247–256
Canli M, Ay O, Kalay M (1998) Levels of heavy metals (Cd, Pb, Cu, Cr and Ni) in tissue of Cyprinus carpio, Barbus capito and Chondrostoma regium from the Seyhan River. Turk J Zool 22:149–157
Cao M, Liu G (2008) Habitat suitability change of red-crowned crane in Yellow River Delta Nature Reserve. J Forestry Res 19(2):141–147
Custer CM, Custer TW, Anteau MJ, Afton AD, Wooten DE (2003) Trace elements in lesser scaup (Aythya affinis) from the Mississippi flyway. Ecotoxicology 12:47–54
Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (1999) Are eggshells and egg contents of great and blue tits suitable as indicators of heavy metal pollution? Belg J Zool 129:439–447
Dauwe T, Janssens E, Kempenaers B, Eens M (2004) The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environ Pollut 129:125–129
Gee GW, Bauder JW (1982) Particle-size analysis. In: Miller RH,Keeney DR (eds) Methods of Soil Analysis: Part 2. Agronomy Monographs: No. 9, 2nd ed. ASA, Madison, 383–411
Degernes LA (2008) Waterfowl toxicology: a review. Veterinary Clinics of North America; Exotic Animal Practice 11:283–300
Fu J, Wang H, Billah SMR, Yu H, Zhang X (2014a) Heavy metals in seawater, sediments, and biota from the coastal area of Yancheng City, China. Environ Toxicol Chem 33:1697–1704
Fu J, Wang Q, Wang H, Yu H, Zhang X (2014b) Monitoring of non-destructive sampling strategies to assess the exposure of avian species in Jiangsu Province, China to heavy metals. Environ Sci Pollut Res 21:2898–2906
Gonzalez LM, Hiralda F (1988) Organochlorine and heavy metal contamination in the eggs of Spanish imperial eagle (Aquila (heliaca) adalberti) and accompanying changes in eggshell morphology and chemistry. Environ Pollut 51:241–258
Hashmi MZ, Malik RN, Shahbaz M (2013) Heavy metals in eggshells of cattle egret (Bubulcu ibis) and little egret (Egretta garzetta) from the Punjab Province, Pakistan. Ecotoxicol Environ Safety 89:158–165
Joint FAO/WHO food standards programme (1990) Guideline levels for cadmium and lead in food. Codex committee of food additives and contamination, 22nd session, Hague, 19–24 March
Kabata-Pendias A (2001) Trace elements in soils and plants (third edition). CRC Press, Boca Raton
Lewis JC, Drewien RC, Kuyt E, Sanchez C (1992) Contaminants in habitat, tissue, and egg of whooping cranes. Proc North Am. Crane Workshop 6:159–165
Luo J, Ye Y, Gao Z, Wang W (2015b) Essential and nonessential elements in red-crowned cranes (Grus japonensis) of Zhalong wetland, northeastern China. Toxicol Environ Chem 96:1096–1105
Luo J, Ye Y, Gao Z, Wang Y, Wang W (2015a) Heavy metal contaminations and influence on the red-crowned crane (Grus japonensis) in Wuyur catchments, northeastern china. Environ Earth Sci 73:5657–5667
Luo J, Yin X, Ye Y, Wang Y, Zang S, Zhou X (2013) Pb and Cd bioaccumulations in the habitat and preys of red-crowned cranes (Grus japonensis) in Zhalong wetland, northeastern China. Biol Trace Elem Res 156:134–143
Ma Y, Li X (2002) Research on the red-crowned crane (Grus japonensis). Shanghai Scientific & Technological Education Press, Shanghai, P.R.China (in Chinese)
MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxic 39:20–31
Miljeteig C, Gabrielsen GW, Strøm H, Gavrilo M (2012) Eggshell thinning and decreased concentrations of vitamin E are associated with contaminants in eggs of ivory gulls. Sci Total Environ 431:92–99
Mora M (2003) Heavy metals and metalloids in egg contents and eggshells of passerine birds from Arizona. Environ Pollu 125:393–400
Negro J, Donázar J, Hiraldo F (1993) Organochlorine and heavy metal contamination in non-viable eggs and its relation to breeding success in a Spanish population of lesser kestrels (Falco naumanni). Environ Pollut 82:201–205
Orłowski G, Kamiński P, Kasprzykowski Z, Zawada Z (2012) Metal interactions within and between tissues of nesting rooks Corvus frugilegus. Biologia 67(6):1211–1219
Orłowski G, Kasprzykowski Z, Dobicki W, Pokorny P, Polechoński R (2010) Geographical and habitat differences in concentrations of copper, zinc and arsenic in eggshells of the rook Corvus frugilegus in Poland. J Ormithol 151:279–286
Orłowski G, Kasprzykowski Z, Zawada Z, Kopij G (2009) Stomach content and grit ingestion by rook Corvus frugilegus nestlings. Ornis Fennica 86:117–122
Orłowski G, Hałupka L (2015a) Embryonic eggshell thickness erosion: a literature survey re-assessing embryo-induced eggshell thinning in birds. Environ Pollut 205:218–224
Orłowski G, Hałupka L, Pokorny P, Klimczuk E, Sztwiertnia H, Dobicki W (2015b) The effect of embryonic development on metal and calcium content in eggs and eggshells in a small passerine. Ibis 158:144–154
Orłowski G, Kasprzykowski Z, Dobicki W, Wuczyński A, Polechoński R (2014) Trace element interactions in rook Corvus frugilegus eggshells along an urbanization gradient. Arch Environ Contam Toxicol 67:519–528
Pain DJ,Meharg AA, FerrerM, TaggartM, Penteriani P. 2005. Lead Concentrations in Bones and Feathers of the Globally Threatened Spanish Imperial Eagle. Biological Conservation 121: 603–610
Scheuhammer AM (1987) The chronic toxicity of aluminum, cadmium, mercury, and lead in bird: a review. Environ Pollut 46:263–295
Scheuhammer AM (1991) Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ Pollut 71:329–375
Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ Pollut 94:337–343
Scheuhammer AM, McNicol DK, Mallory ML, Kerekes JJ (1997) Relationships between lake chemistry and calcium and trace elements concentrations of aquatic invertebrates eaten by breeding insectivorous waterfowl. Environ Pollut 96:235–247
Sekabira K, Oryem O, Basamba T, Mutumba G, Kakudidi E (2010) Assessment of heavy metal pollution in the urban stream sediments and its tributaries. Int J Environ Sci Tech 7:435–446
Skalká M, Koréneková B, Nad P, Śály J (2008) Influence of chromium and cadmium addition on quality of Japanese quail eggs. Acta Vet Brno 77:503–508
Su L, Zhou F (2012) Status, threats and conservation needs for the continental population of the red-crowned crane. China Birds 3:147–164
Wiemeyer SN, Withers D (2004) Metals and trace elements in livers of American white pelicans at Anaho Island. Nevada 2004 United States Fish and Wildlife Service, Nevada
Zduniak P (2005) Forced regurgitation with tartar emetic as an effective and safe method to study diet composition in hooded crow nestlings. Eur J Wildl Res 51:122–125
Zhong X, Zhou S, Zhu Q, Zhao Q (2011) Fraction distribution and bioavailability of soil heavy metals in the Yangtze River Delta—a case of Kunshan City in Jiangshu Province, China. J Hazard Mater 198:13–21
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This research was supported by the Heilongjiang Provincial Nature Fund of China (Grant No. C2016058).
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Jinming, L., Yongjie, W., Zhongyan, G. et al. The excessive enrichment of trace elements in migratory and breeding red-crowned cranes (Grus japonensis) in China. Environ Sci Pollut Res 24, 16351–16363 (2017). https://doi.org/10.1007/s11356-017-9258-0
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DOI: https://doi.org/10.1007/s11356-017-9258-0