Abstract
We examined how variation in MeHg concentrations through time is reflected in birds, a taxon commonly used as a biological indicator of ecosystem health. Using museum specimens collected from 1880 to 2016, we measured feather MeHg concentrations in six species of birds that breed in New York State and have distinct dietary and habitat preferences. We predicted that MeHg concentrations in feathers would mirror Hg emission patterns in New York State and increase through time until 1980 then decrease thereafter in response to increased regulation of anthropogenic Hg emissions. We found that MeHg concentrations increased with δ15N, and that MeHg feather concentrations for some individuals from four of the six species examined exceeded concentrations known to cause negative sublethal effects in birds. In contrast to our prediction, MeHg concentrations in feathers did not parallel global or local Hg emissions through time and varied by species, even after controlling for possible changes in diet and habitat. MeHg concentrations varied substantially within species and individual specimens, suggesting that high within-individual variation in feather MeHg concentrations caused by spatiotemporal variation in molt, environmental Hg exposure, or mobility decoupling Hg uptake from breeding sites, may obscure trends in MeHg through time. Our study provides a unique assessment of feather MeHg in six species not typically analyzed using this retrospective approach.
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References
Appelquist H, Drabæk I, Asbirk S (1985) Variation in mercury content of guillemot feathers over 150 years. Mar Pollut Bull 16:244–248. https://doi.org/10.1016/0025-326X(85)90509-0
Baron LA, Ashwood TL, Sample BE, Welsh C (1997) Monitoring bioaccumulation of contaminants in the belted kingfisher (Ceryle alcyon). Environ Monit Assess 47:153–165. https://doi.org/10.1023/A:1005812131961
Becker DS, Bigham GN (1995) Distribution of mercury in the aquatic food web of Onondaga Lake, New York. Water Air Soil Pollut 80:563–571. https://doi.org/10.1007/bf01189706
Bond AL, Diamond AW (2008) High within-individual variation in total mercury concentrations in seabird feathers. Environ Toxicol Chem 27:2375–2377. https://doi.org/10.1897/08-163.1
Bond AL, Hobson KA, Branfireun BA (2015) Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc R Soc B Biol Sci 282:20150032–20150032. https://doi.org/10.1098/rspb.2015.0032
Bortolotti GR (2010) Flaws and pitfalls in the chemical analysis of feathers: bad news–good news for avian chemoecology and toxicology. Ecol Appl 20:1766–1774. https://doi.org/10.1890/09-1473.1
Bourbour RP, Martinico BL, Ackerman JT, Herzog MP, Hull AC, Fish AM, Hull JM (2019) Feather mercury concentrations in North American raptors sampled at migration monitoring stations. Ecotoxicology 28:379–391. https://doi.org/10.1007/s10646-019-02016-2
Braune BM, Malone BJ (2006) Organochlorines and trace elements in upland game birds harvested in Canada. Sci Total Environ 363:60–69. https://doi.org/10.1016/j.scitotenv.2005.06.011
Burger J (2013) Temporal trends (1989-2011) in levels of mercury and other heavy metals in feathers of fledgling great egrets nesting in Barnegat Bay, NJ. Environ Res 122:11–17. https://doi.org/10.1016/j.envres.2013.01.003
Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172. https://doi.org/10.1006/enrs.1997.3778
Cain A, Morgan JT, Brooks N (2011) Mercury policy in the Great Lakes states: past successes and future opportunities. Ecotoxicology 20:1500–1511. https://doi.org/10.1007/s10646-011-0764-4
Carravieri A, Bustamante P, Churlaud C, Fromant A, Cherel Y (2014) Moulting patterns drive within-individual variations of stable isotopes and mercury in seabird body feathers: implications for monitoring of the marine environment. Mar Biol 161:963–968. https://doi.org/10.1007/s00227-014-2394-x
Champoux L, Masse DC, Evers DC, Lane O, Plante M, Timmerman STA (2006) Assessment of mercury exposure and potential effects on common loons (Gavia immer) in Quebec. Hydrobiologia 567:263–274. https://doi.org/10.1007/s10750-006-0066-7
Conway, CJ (1995) Virginia rail (Rallus limicola), the birds of north america online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/virrai. Accessed 20 Mar 2017
Cristol DA, Savoy L, Evers DC, Perkins C, Taylor R, Varian‐Ramos CW (2012) Mercury in waterfowl from a contaminated river in Virginia. J Wildl Manag 76:1617–1624. https://doi.org/10.1002/jwmg.430
Curtis OE, Rosenfield RN, Bielefeldt J (2006) Cooper’s hawk (Accipiter cooperii), the birds of North America online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/coohaw. Accessed 20 Mar 2017
Dietz R, Riget FF, Boertmann D, Sonne C, Olsen MT, Fjeldsa J, Falk K, Kirkegaard M, Egevang C, Asmund G, Wille F, Møller S (2006) Time trends of mercury in feathers of West Greenland birds of prey during 1851-2003. Environ Sci Technol 40:5911–5916. https://doi.org/10.1021/es0609856
Dmowski K (1999) Birds as bioindicators of heavy metal pollution: review and examples concerning European species. Acta Ornithol 34:1–25
Eagles-Smith CA, Ackerman JT, Adelsbach TL, Takekawa JY, Miles AK, Keister RA (2008) Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA. Environ Toxicol Chem 27:2136–2153. https://doi.org/10.1897/08-038.1
Eisler R (1987) Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 85(1.10)
Evans RJ, Bails JD, D’Ltri FM (1972) Mercury levels in muscle tissues of preserved museum fish. Environ Sci Technol 6:901–905. https://doi.org/10.1021/es60069a007
Evers DC, Burgess N, Champoux L, Hoskins B, Major A, Goodale W, Taylor R, Poppenga R, Daigle T (2005) Patterns of mercury exposure in the avian community of northeastern North America. Ecotoxicology 14:193–221. https://doi.org/10.1007/s10646-004-6269-7
Evers DC, Savoy LJ, Desorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH, Bank MS, Major A, Munney K, Mower BF, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81. https://doi.org/10.1007/s10646-007-0168-7
Evers DC, Schmutz JA, Basu N, DeSorbo CR, Fair J, Gray CE, Paruk JD, Perkins M, Regan K, Uher-Koch BD, Wright KG (2014) Historic and contemporary mercury exposure and potential risk to yellow-billed loons (Gavia adamsii) breeding in Alaska and Canada. Waterbirds 37:147–159. https://doi.org/10.1675/063.037.sp117
Evers DC, Wiener JG, Basu N, Bodaly RA, Morrison HA, Williams KA (2011) Mercury in the Great Lakes region: bioaccumulation, spatiotemporal patterns, ecological risks, and policy. Ecotoxicology 20:1487–1499. https://doi.org/10.1007/s10646-011-0784-0
Frederick PC, Hylton B, Heath JA, Spalding MG (2004) A historical record of mercury contamination in Southern Florida (USA) as inferred from avian feather tissue. Environ Toxicol Chem 23:1474–1478. https://doi.org/10.1897/03-403
Gilmour CC, Henry EA, Ralph M (1992) Sulfate stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–2287. https://doi.org/10.1021/es00035a029
Goodale MW, Evers DC, Mierzykowski SE, Bond AL, Burgess NM, Otorowski CI, Welch LJ, Hall CS, Ellis JC, Allen RB, Diamond AW, Kress SW, Taylor RJ (2008) Marine foraging birds as bioindicators of mercury in the Gulf of Maine. Ecohealth 5:409–425. https://doi.org/10.1007/s10393-009-0211-7
Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161. https://doi.org/10.1525/auk.2009.09058
Head JA, Debofsky A, Hinshaw J, Basu N (2011) Retrospective analysis of mercury content in feathers of birds collected from the state of Michigan (1895-2007). Ecotoxicology 20:1636–1643. https://doi.org/10.1007/s10646-011-0738-6
Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 56:129–138. https://doi.org/10.1007/s00244-008-9160-3
Hepp GR, Bellrose FC (2013) Wood duck (Aix sponsa), the birds of North America online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/wooduc. Accessed 20 Mar 2017
Hindell MA, Brothers N, Gales R (1999) Mercury and cadmium concentrations in the tissues of three species of southern albatrosses. Polar Biol 22:102–108. https://doi.org/10.1007/s003000050396
Hollamby S, Afema-Azikuru J, Sikarskie JG, Kaneene JB, Bowerman WW, Fitzgerald SD, Cameron K, Gandolf AR, Hui GN, Dranzoa C, Rumbeiha WK (2004) Mercury and persistent organic pollutant concentrations in african fish eagles, marabou sotriks, and nile tilapia in Uganda. J Wildl Dis 40:501–514. https://doi.org/10.7589/0090-3558-40.3.501
Ikemoto T, Kunito T, Tanaka H, Baba N, Miyazaki N, Tanabe S (2004) Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch Environ Contam Toxicol 47:402–413. https://doi.org/10.1007/s00244-004-3188-9
Jackson A, Evers DC, Eagles-Smith CA, Ackerman JT, Willacker JJ, Elliott JE, Lepak JM, Vander Pol SS, Bryan CE (2016) Mercury risk to avian piscivores across western United States and Canada. Sci Total Environ 568:685–696. https://doi.org/10.1016/j.scitotenv.2016.02.197
Jackson AK, Evers DC, Adams EM, Cristol DA, Eagles-Smith C, Edmonds ST, Gray CE, Hoskins B, Lane OP, Sauer A, Tear T (2015) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467. https://doi.org/10.1007/s10646-014-1394-4
Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA (2011) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the carolina wren (Thryothorus ludovicianus). Auk 128:759–769. https://doi.org/10.1525/auk.2011.11106
Keller RH, **e L, Buchwalter DB, Franzreb KE, Simons TR (2014) Mercury bioaccumulation in Southern Appalachian birds, assessed through feather concentrations. Ecotoxicology 23:304–316. https://doi.org/10.1007/s10646-013-1174-6
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27. https://doi.org/10.1139/z99-165
Kelly JF, Bridge ES, Hamas MJ (2009) Belted Kingfisher (Megaceryle alcyon), the birds of North America online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/belkin1. Accessed 20 Mar 2017
Kopec AD, Bodaly RA, Lane OP, Evers DC, Leppold AJ, Mittelhauser GH (2018) Elevated mercury in blood and feathers of breeding marsh birds along the contaminated lower Penobscot River, Maine, USA. Sci Total Environ 634:1563–1579. https://doi.org/10.1016/j.scitotenv.2018.03.223
Kushlan JA (1993) Colonial waterbirds as bioindicators of environmental change. Colon Waterbird 16:223–251
Lavoie RA, Baird CJ, King LE, Kyser TK, Friesen VL, Campbell LM (2014) Contamination of mercury during the wintering period influences concentrations at breeding sites in two migratory piscivorous birds. Environ Sci Technol 48:13694–13702. https://doi.org/10.1021/es502746z
Lindsay RC, Dimmick RW (1983) Mercury residues in wood ducks and wood duck foods in eastern Tennessee. J Wildl Dis 19:114–117. https://doi.org/10.7589/0090-3558-19.2.114
Lindstedt SL, Calder WA (1976) Body size and longevity in birds. Condor 78:91–94
Lourenço R, Tavares PC, Del Mar Delgado M, Rabaça JE, Penteriani V (2011) Superpredation increases mercury levels in a generalist top predator, the eagle owl. Ecotoxicology 20:635–642. https://doi.org/10.1007/s10646-011-0603-7
Low KE, Ramsden DK, Jackson AK, Emery C, Robinson WD, Randolph J, Eagles-Smith CA (2019) Songbird feathers as indicators of mercury exposure: high variability and low predictive power suggest limitations. Ecotoxicology. https://doi.org/10.1007/s10646-019-02052-y
Martínez Fernández J, Esteve Selma MA, Aymerich FR, Pardo Sáez MT, Carreño Fructuoso MF (2005) Aquatic birds as bioindicators of trophic changes and ecosystem deterioration in the Mar Menor lagoon (SE Spain). Hydrobiologia 550:221–235. https://doi.org/10.1007/s10750-005-4382-0
Marvin C, Painter S, Rossmann R (2004) Spatial and temporal patterns in mercury contamination in sediments of the Laurentian Great Lakes. Environ Res 95:351–362. https://doi.org/10.1016/j.envres.2003.09.007
McCullagh EA, Cristol DA, Phillips JB (2015) Plumage color and reproductive output of eastern bluebirds (Sialia sialis) nesting near a mercury-contaminated river. J Environ Sci Heal 50:1020–1028. https://doi.org/10.1080/10934529.2015.1038168
Newman MC, Xu X, Condon A, Liang L (2011) Floodplain methylmercury biomagnification factor higher than that of the contiguous river (South River, Virginia USA). Environ Pollut 159:2840–2844. https://doi.org/10.1016/j.envpol.2011.04.045
Paritte JM, Kelly JF (2009) Effect of cleaning regime on stable-isotope ratios of feathers in japanese quail (Coturnix japonica). Auk 126:165–174. https://doi.org/10.1525/auk.2009.07187
Pedro S, Xavier JC, Tavares S, Trathan PN, Ratcliffe N, Paiva VH, Medeiros R, Pereira E, Pardal MA (2015) Feathers as a tool to assess mercury contamination in gentoo penguins: variations at the individual level. PLoS One 10:1–8. https://doi.org/10.1371/journal.pone.0137622
Perkins M, Lane OP, Evers DC, Sauer A, Adams EM, O’Driscoll NJ, Edmunds ST, Jackson AK, Hagelin JC, Trimble J, Sunderland EM (2019) Historical patterns in mercury exposure for North American songbirds. Ecotoxicology
Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282. https://doi.org/10.1111/j.2041-210X.2010.00061.x
Pirrone N, Allegrini I, Keeler GJ, Nriagu JO, Rossmann R, Robbins JA (1998) Historical atmospheric mercury emissions and depositions in North America compared to mercury accumulations in sedimentary records. Atmos Environ 32:929–940. https://doi.org/10.1016/S1352-2310(97)00353-1
Pirrone N, Cinnirella S, Feng X, Finkelman RB, Friedli HR, Leaner J, Mason R, Mukherjee AB, Stracher GB, Streets DG, Telmer K (2010) Global mercury emissions to the atmosphere from anthropogenic and natural sources. Atmos Chem Phys 10:5951–5964. https://doi.org/10.5194/acp-10-5951-2010
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. ISBN 3-900051-07-0. http://www.R-project.org
Rohwer S, Ricklefs RE, Rohwer VG, Copple MM (2009) Allometry of the duration of flight feather molt in birds. PLoS Biol 7:e100012. https://doi.org/10.1371/journal.pbio.1000132
Rusch, DH, Destefano, Reynolds MC, Lauten D (2000) Ruffed grouse (Bonasa umbellus), the birds of North America online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/rufgro. Accessed 20 Mar 2018
Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295. https://doi.org/10.1016/0269-7491(87)90173-4
Streets DG, Devane MK, Lu Z, Bond TC, Sunderland EM, Jacob DJ (2011) All-time releases of mercury to the atmosphere from human activities. Environ Sci Technol 45:10485–10491. https://doi.org/10.1021/es202765m
Streets DG, Horowitz HM, Jacob DJ, Lu Z, Levin L, Ter Schure AFH, Sunderland EM (2017) Total mercury released to the environment by human activities. Environ Sci Technol 51:5969–5977. https://doi.org/10.1021/acs.est.7b00451
Strekopytov S, Brownscombe W, Lapinee C, Sykes D, Spratt J, Jeffries TE, Jones CG (2017) Arsenic and mercury in bird feathers: identification and quantification of inorganic pesticide residues in natural history collections using multiple analytical and imaging techniques. Microchem J 130:301–309. https://doi.org/10.1016/j.microc.2016.10.009
Thompson DR, Furness RW, Lewis SA (1993) Temporal and spatial variation in mercury concentrations in some albatrosses and petrels from the sub-Antarctic. Polar Biol 13:239–244. https://doi.org/10.1007/BF00238759
Thompson DR, Furness RW, Walsh PM (1992) Historical changes in mercury concentrations in the marine ecosystem of the North and North-East Atlantic Ocean as indicated by seabird feathers. J Appl Ecol 29:79–84. https://doi.org/10.2307/2404350
USEPA (1998) Method 1630. Methyl mercury in water by distillation, aqueous ethylation, purge and trap, and CVAFS. US Environmental Protection Agency, Washington, DC
Ullrich SM, Tanton TW, Abdrashitova SA (2001) Mercury in the aquatic environment: a review of factors affecting methylation. Crit Rev Environ Sci Technol 31:241–293. https://doi.org/10.1080/20016491089226
Vo A-TE, Bank MS, Shine JP, Edwards SV (2011) Temporal increase in organic mercury in an endangered pelagic seabird assessed by century-old museum specimens. Proc Natl Acad Sci 108:7466–7471. https://doi.org/10.1073/pnas.1013865108
Weeks HP (2011). Eastern phoebe (Sayornis phoebe), the birds of North America online. Cornell Lab of Ornithology. https://birdsna.org/Species-Account/bna/species/easpho. Accessed 20 March 2018
Weseloh DVC, Moore DJ, Hebert CE, De Solla SR, Braune BM, McGoldrick DJ (2011) Current concentrations and spatial and temporal trends in mercury in Great Lakes herring gull eggs, 1974-2009. Ecotoxicology 20:1644–1658. https://doi.org/10.1007/s10646-011-0755-5
White AE, Cristol DA (2014) Plumage coloration in belted kingfishers (Megaceryle alcyon) at a mercury-contaminated river. Waterbirds 37:144–152. https://doi.org/10.1675/063.037.0203
Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146. https://doi.org/10.1002/etc.5620170203
Zhou C, Cohen MD, Crimmins BA, Zhou H, Johnson TA, Hopke PK, Holsen TM (2017) Mercury temporal trends in top predator fish of the Laurentian Great Lakes from 2004 to 2015: are concentrations still decreasing? Environ Sci Technol 51:7386–7394. https://doi.org/10.1021/acs.est.7b00982
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, NY
Acknowledgements
A special thanks to Dr. David Bonter and his lab group, as well as Dr. Alex Flecker, Kimberlee L. Sparks, and Dr. Irby Lovette for their help and encouragement. Comments from three anonymous reviewers helped clarify and refine earlier versions of this paper. Paul Sweet at the American Museum of Natural History and Dr. Jeremy Kirchman at the New York State Museum very kindly provided access to specimens for this work. Statistical assistance from the Cornell Statistical Consulting Unit (CSCU) and Sarah “T” Toner was greatly appreciated. We would also like to thank Mark Burton at the Biodiversity Research Institute for updating the map figure. Additional recognition is due to Cornell University, the Finger Lakes Institute at Hobart and William Smith Colleges, the Cornell Lab of Ornithology, the National Science Foundation, and the Cornell Redheads Fund for financial support and resources. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE1534175. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.
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Dzielski, S.A., Razavi, N.R., Twining, C.W. et al. Reconstructing avian mercury concentrations through time using museum specimens from New York State. Ecotoxicology 29, 1802–1814 (2020). https://doi.org/10.1007/s10646-019-02123-0
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DOI: https://doi.org/10.1007/s10646-019-02123-0