Interactions Between Heavy Metal Exposure and Blood Biochemistry in an Urban Population of the Black Swan (Cygnus atratus) in Australia.
Journal
Archives of environmental contamination and toxicology
ISSN: 1432-0703
Titre abrégé: Arch Environ Contam Toxicol
Pays: United States
ID NLM: 0357245
Informations de publication
Date de publication:
21 Feb 2024
21 Feb 2024
Historique:
received:
21
08
2023
accepted:
02
02
2024
medline:
22
2
2024
pubmed:
22
2
2024
entrez:
21
2
2024
Statut:
aheadofprint
Résumé
There is growing recognition of the threat posed to wildlife by pollutants. Waterbirds are robust bioindicators of ecosystem health, and metal toxicity is a threat to these species in waterways worldwide. Urban waterbirds are likely to be at the highest risk of heavy metal exposure, but this issue has not been widely explored in Australia. Our aim was to estimate contemporary heavy metal exposure in a sedentary urban waterbird population: black swans (Cygnus atratus) inhabiting an inner-city wetland in one of Australia's largest cities, Melbourne. To investigate the physiological implications of legacy heavy metal exposure in these birds, we quantified blood biochemistry profiles and examined their relationships with metal concentrations in feathers. We caught 15 swans in 2021 and took feather samples to measure the concentration of eight heavy metals (chromium (Cr), manganese (Mn), iron (Fe), nickel (Ni), copper (Cu), zinc (Zn), lead (Pb), and mercury (Hg)), and blood samples to measure the concentration of 13 plasma analytes. Multivariate regression analysis revealed few associations between heavy metals and biochemistry markers, and no differences between sexes or age classes. This study presents a baseline dataset of these contaminants and blood biochemical profiles of swans at this wetland that can be used for future monitoring and is an important step toward a better understanding of the threat posed by heavy metals to Australian urban waterbirds.
Identifiants
pubmed: 38383776
doi: 10.1007/s00244-024-01055-z
pii: 10.1007/s00244-024-01055-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Ahmadpour M, Lan-Hai L, Ahmadpour M, Hoseini SH, Mashrofeh A, Binkowski ŁJ (2016) Mercury concentration in the feathers of birds from various trophic levels in fereydunkenar international wetland (Iran). Environ Monit Assess 188(12):666
pubmed: 27838877
pmcid: 5107202
doi: 10.1007/s10661-016-5671-y
Albert C, Renedo M, Bustamante P, Fort J (2019) Using blood and feathers to investigate large-scale Hg contamination in Arctic seabirds: a review. Environ Res 177:108588
pubmed: 31382127
doi: 10.1016/j.envres.2019.108588
Al-Daraji HJ, Amen MHM (2011) Effect of dietary zinc on certain blood traits of broiler breeder chickens. Int J Poult Sci 10(10):807–813
doi: 10.3923/ijps.2011.807.813
Aloupi M, Ferentinou E, Zaharaki O-M, Akriotis T (2020) Does dilute nitric acid improve the removal of exogenous heavy metals from feathers? A comparative study towards the optimization of the cleaning procedure of feather samples prior to metal analysis. Ecotoxicol Environ Saf 200:110759
pubmed: 32470677
doi: 10.1016/j.ecoenv.2020.110759
Amat JA, Green AJ (2010) Waterbirds as bioindicators of environmental conditions. In: Hurford C, Schneider M, Cowx I (eds) Conservation Monitoring in Freshwater Habitats. Springer, New York City, USA, pp 45–52
doi: 10.1007/978-1-4020-9278-7_5
Andrade R, Bateman HL, Franklin J, Allen D (2018) Waterbird community composition, abundance, and diversity along an urban gradient. Landsc Urban Plan 170:103–111
doi: 10.1016/j.landurbplan.2017.11.003
Artacho P, Soto-Gamboa M, Verdugo C, Nespolo RF (2007) Blood biochemistry reveals malnutrition in black-necked swans (Cygnus melanocoryphus) living in a conservation priority area. Comp Biochem Physiol a: Mol Integr Physiol 146(2):283–290
pubmed: 17158079
doi: 10.1016/j.cbpa.2006.10.031
Aulsebrook AE, Lesku JA, Mulder RA, Goymann W, Vyssotski AL, Jones TM (2020) Streetlights disrupt night-time sleep in urban black swans. Front Ecol Evol 8:131
doi: 10.3389/fevo.2020.00131
Bates DM (2010) Linear mixed-effects models using “Eigen” and S4. Springer, New York City, USA
Bottini CLJ, MacDougall-Shackleton SA, Branfireun BA, Hobson KA (2021) Feathers accurately reflect blood mercury at time of feather growth in a songbird. Sci Total Environ 775:145739
pubmed: 33621875
doi: 10.1016/j.scitotenv.2021.145739
Bradl HB (2005) Sources and origins of heavy metals. In: Bradl HB (ed) Interface science and technology. Elsevier Science & Technology, Amsterdam, pp 1–27
Brugge D, Durant JL, Rioux C (2007) Near-highway pollutants in motor vehicle exhaust: a review of epidemiologic evidence of cardiac and pulmonary health risks. Environ Health 6(1):23
pubmed: 17688699
pmcid: 1971259
doi: 10.1186/1476-069X-6-23
Burger J, Gochfeld M, Jeitner C et al (2009) Mercury and other metals in eggs and feathers of glaucous-winged gulls (Larus glaucescens) in the Aleutians. Environ Monit Assess 152(1–4):179–194
pubmed: 18626778
doi: 10.1007/s10661-008-0306-6
Carpenter JW, Andrews GA, Beyer WN (2004) Zinc toxicosis in a free-flying trumpeter swan (Cygnus buccinator). J Wildl Dis 40(4):769–774
pubmed: 15650098
doi: 10.7589/0090-3558-40.4.769
Dean CE, Hargis BM, Hargis PS (1991) Effects of zinc toxicity on thyroid function and histology in broiler chicks. Toxicol Lett 57(3):309–318
pubmed: 1882390
doi: 10.1016/0378-4274(91)90205-K
Dear EJ, Guay P-J, Robinson RW, Weston MA (2015) Distance from shore positively influences alert distance in three wetland bird species. Wetlands Ecol Manage 23(2):315–318
doi: 10.1007/s11273-014-9376-0
Degernes L, Heilman S, Trogdon M et al (2006) Epidemiologic investigation of lead poisoning in trumpeter and tundra swans in Washington state, USA, 2000–2002. J Wildl Dis 42(2):345–358
pubmed: 16870857
doi: 10.7589/0090-3558-42.2.345
Douglas TK, Weston MA, Greenwell CN et al (2022) Research methods for birds. In: Smith BP, Waudby HP, Alberthsen C, Hampton JO (eds) Wildlife research in Australia: practical abd applied methods. CSIRO Publishing, Melbourne, Australia, pp 313–359
Evans MN, Waller S, Müller CT et al (2022) The price of persistence: assessing the drivers and health implications of metal levels in indicator carnivores inhabiting an agriculturally fragmented landscape. Environ Res 207:112216
pubmed: 34656630
doi: 10.1016/j.envres.2021.112216
Finger A, Lavers JL, Orbell JD, Dann P, Nugegoda D, Scarpaci C (2016) Seasonal variation and annual trends of metals and metalloids in the blood of the little penguin (Eudyptula minor). Mar Pollut Bull 110(1):261–273
pubmed: 27329818
doi: 10.1016/j.marpolbul.2016.06.055
Gasaway WC, Buss IO (1972) Zinc toxicity in the mallard duck. J Wildl Manag 36(4):1107–1117
doi: 10.2307/3799239
Golden NH, Rattner BA, Cohen JB, Hoffman DJ, Russek-Cohen E, Ottinger MA (2003) Lead accumulation in feathers of nestling black-crowned night herons (Nycticorax nycticorax) experimentally treated in the field. Environ Toxicol Chem 22(7):1517–1524
pubmed: 12836976
Green AJ, Elmberg J (2014) Ecosystem services provided by waterbirds. Biol Rev 89(1):105–122
pubmed: 23786594
doi: 10.1111/brv.12045
Green AJ, Alcorlo P, Peeters ETHM et al (2017) Creating a safe operating space for wetlands in a changing climate. Front Ecol Environ 15(2):99–107
doi: 10.1002/fee.1459
Grier JW (1982) Ban of DDT and subsequent recovery of reproduction in bald eagles [Haliaeetus leucocephalus, Canada]. Science 218(4578):1232–1235
pubmed: 7146905
doi: 10.1126/science.7146905
Grúz A, Szemerédy G, Kormos É et al (2015) Monitoring of heavy metal burden in mute swan (Cygnus olor). Environ Sci Pollut Res 22(20):15903–15909
doi: 10.1007/s11356-015-4809-8
Guay P-J, Mulder R (2009) Do neck-collars affect the behaviour and condition of Black Swans (Cygnus atratus)? Emu-Austr Ornithol 109(3):248–251
doi: 10.1071/MU09020
Harper M, Hindmarsh M (1990) Lead poisoning in magpie geese Anseranas semipalmata from ingested lead pellet at bool lagoon game reserve (South Australia). Wildl Res 17(2):141–145
doi: 10.1071/WR9900141
Harris DJ (2009) Clinical tests. In: Tully TN, Dorrestein GM, Jones AK, Cooper JE (eds) Handbook of avian medicine, 2nd edn. WB Saunders, Edinburgh, pp 77–84
doi: 10.1016/B978-0-7020-2874-8.00004-3
Jaspers V, Dauwe T, Pinxten R et al (2004) The importance of exogenous contamination on heavy metal levels in bird feathers. A field experiment with free-living great tits, Parus major. J Environ Monit 6(4):356–356
pubmed: 15054546
doi: 10.1039/b314919f
Kaya S, Keçeci T, Haliloğlu S (2001) Effects of zinc and vitamin A supplements on plasma levels of thyroid hormones, cholesterol, glucose and egg yolk cholesterol of laying hens. Res Vet Sci 71(2):135–139
pubmed: 11883892
doi: 10.1053/rvsc.2001.0500
Koh T, Harper M (1988) Lead poisoning in black swans, Cygnus atratus, exposed to spent lead shot at bool lagoon game reserve. South Austr Wildl Res 15(4):395–403
doi: 10.1071/WR9880395
Kraaijeveld K, Carew P, Billing T, Adcock GJ, Mulder RA (2004) Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus). Mol Ecol 13(6):1625–1633
pubmed: 15140105
doi: 10.1111/j.1365-294X.2004.02172.x
Kucuk O, Sahin N, Sahin K (2003) Supplemental zinc and vitamin A can alleviate negative effects of heat stress in broiler chickens. Biol Trace Elem Res 94(3):225–235
pubmed: 12972690
doi: 10.1385/BTER:94:3:225
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25(1):1–18
doi: 10.18637/jss.v025.i01
Lettoof D, Rankenburg K, McDonald B et al (2021) Snake scales record environmental metal (loid) contamination. Environ Pollut 274:116547
pubmed: 33548672
doi: 10.1016/j.envpol.2021.116547
Martinez-Finley EJ, Aschner M (2014) Recent advances in mercury research. Curr Environ Health Reports 1(2):163–171
doi: 10.1007/s40572-014-0014-z
Martinez-Haro M, Green AJ, Mateo R (2011) Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environ Res 111(4):530–538
pubmed: 21411076
doi: 10.1016/j.envres.2011.02.012
McCall KA, Huang C-c, Fierke CA (2000) Function and mechanism of zinc metalloenzymes. J Nutr 130(5):1437S-1446S
pubmed: 10801957
doi: 10.1093/jn/130.5.1437S
McCurdy E (2011) Successful low level mercury analysis using the Agilent 7700 series ICP-MS. Agilent ICP-MS Journal:45
Meissner W, Binkowski ŁJ, Barker J, Hahn A, Trzeciak M (2020) Relationship between blood lead levels and physiological stress in mute swans (Cygnus olor) in municipal beaches of the southern Baltic. Sci Total Environ 710:136292
pubmed: 32050362
doi: 10.1016/j.scitotenv.2019.136292
Milani JF, Wilson H, Ziccardi M, LeFebvre R, Scott C (2012) Hematology, plasma chemistry, and bacteriology of wild tundra swans (Cygnus columbianus) in Alaska. J Wildl Dis 48(1):212–215
pubmed: 22247394
doi: 10.7589/0090-3558-48.1.212
National Health and Medical Research Council (2013) australian code for the care and use of animals for scientific purposes. In: 8th edn. National health and medical research council, Canberra, Australia
Nie D, Gui J, Zhao N et al (2020) Haematological and serum biochemical reference values in Chinese water deer (Hydropotes inermis): a preliminary study. BMC Vet Res 16(1):395–395
pubmed: 33081761
pmcid: 7574586
doi: 10.1186/s12917-020-02601-2
Nzabanita D, Hampton JO, Toop SD et al (2023a) Expanding the use of portable XRF to monitor lead exposure in an Australian duck species two decades after a ban on lead shot. Sci Total Environ 869:161803
pubmed: 36708833
doi: 10.1016/j.scitotenv.2023.161803
Nzabanita D, Shen H, Grist S et al (2023b) Exposure to POPs in Australian waterbirds. Environ Toxicol Chem. https://doi.org/10.1002/etc.5804
doi: 10.1002/etc.5804
pubmed: 38085117
O’Halloran J, Duggan PF, Myers AA (1988) Biochemical and haematological values for mute swans (Cygnus olor): effects of acute lead poisoning. Avian Pathol 17(3):667–678
pubmed: 18766723
doi: 10.1080/03079458808436484
Parak T, Strakova E (2011) Zinc as a feed supplement and its impact on plasma cholesterol concentrations in breeding cocks. Acta Vet Brno 80(3):281–285
doi: 10.2754/avb201180030281
Payne CJ, Jessop TS, Guay P-J, Johnstone M, Feore M, Mulder RA (2012) Population, behavioural and physiological responses of an urban population of black swans to an intense annual noise event. PLoS ONE 7(9):e45014
pubmed: 23024783
pmcid: 3443219
doi: 10.1371/journal.pone.0045014
Philpot SM, Lavers JL, Nugegoda D, Gilmour ME, Hutton I, Bond AL (2019) Trace element concentrations in feathers of seven petrels (Pterodroma spp.). Environ Sci Pollut Res 26(10):9640–9648
doi: 10.1007/s11356-019-04406-9
Porter J, Spencer J, O’Neill S, Brandis KJ, Watson MJ (2022) Aquatic birds. In: Smith BP, Waudby HP, Alberthsen C, Hampton JO (eds) Wildlife research in Australia: practical and applied methods. CSIRO, Melbourne, Australia, pp 599–608
Sayadi MH, Sayyed MRG, Kumar S (2010) Short-term accumulative signatures of heavy metals in river bed sediments in the industrial area, Tehran. Iran Environ Monitor Assess 162(1–4):465–473
doi: 10.1007/s10661-009-0810-3
Seewagen CL (2010) Threats of environmental mercury to birds: knowledge gaps and priorities for future research. Bird Conserv Int 20(2):112–123
doi: 10.1017/S095927090999030X
Shah M, Zaneb H, Masood S et al (2020) Effect of single or combined supplementation of zinc and probiotics on muscle and bone characteristics and haematobiochemical profile in broilers. Veterinární Medicína 65(3):134–142
doi: 10.17221/152/2019-VETMED
Smith AN, Vernes KA, Ford HA (2012) Grazing effects of Black Swans Cygnus atratus (Latham) on a seasonally flooded coastal wetland of eastern Australia. Hydrobiologia 697:45–57
doi: 10.1007/s10750-012-1169-y
Szabo D, Moodie D, Green MP, Mulder RA, Clarke BO (2022) Field-based distribution and bioaccumulation factors for cyclic and aliphatic per-and polyfluoroalkyl substances (PFASs) in an urban sedentary waterbird population. Environ Sci Technol 56(12):8231–8244
pubmed: 35678721
doi: 10.1021/acs.est.2c01965
United Nations (2021) What is the Triple Planetary Crisis? United Nations framework convention on climate change, New York City, USA. Report available on-line at: https://unfccc.int/blog/what-is-the-triple-planetary-crisis
Varian-Ramos CW, Swaddle JP, Cristol DA (2014) Mercury reduces avian reproductive success and imposes selection: an experimental study with adult- or lifetime-exposure in zebra finch. PLoS ONE 9(4):e95674
pubmed: 24759822
pmcid: 3997408
doi: 10.1371/journal.pone.0095674
Vizuete J, Pérez-López M, Míguez-Santiyán MP, Hernández-Moreno D (2019) Mercury (Hg), lead (Pb), cadmium (Cd), selenium (Se), and arsenic (As) in liver, kidney, and feathers of gulls: a review. Rev Environ Contam Toxicol 247:85–146
pubmed: 30413976
Walker CH, Sibly RM, Hopkin SP, Peakall DB (2012) Principles of ecotoxicology, 4th edn. CRC Press, Boca Raton, USA
Wang F, Xu S, Zhou Y, Wang P, Zhang X (2017) Trace element exposure of whooper swans (Cygnus cygnus) wintering in a marine lagoon (Swan Lake), northern China. Mar Pollut Bull 119(2):60–67
pubmed: 28392089
doi: 10.1016/j.marpolbul.2017.03.063
Whitney MC, Cristol DA (2018) Impacts of sublethal mercury exposure on birds: a detailed review. In: de Voogt P (ed) Reviews of environmental contamination and toxicology, vol 244. Springer International Publishing. Cham, Switzerland, pp 113–163
Wickson R, Norman F, Bacher G, Garnham J (1992) Concentrations of lead in bone and other tissues of Victorian waterfowl. Wildl Res 19(2):221–231
doi: 10.1071/WR9920221
Williams M (1973) Mortality of the black swan in New Zealand-a progress report. Wildfowl 24(24):54–55
Ye R, Tan C, Chen B, Li R, Mao Z (2020) Zinc-containing metalloenzymes: inhibition by metal-based anticancer agents. Front Chem 8:402–402
pubmed: 32509730
pmcid: 7248183
doi: 10.3389/fchem.2020.00402