Sex differences in mercury contamination of birds: testing multiple hypotheses with meta-analysis.

The sex of a bird can, in principle, affect exposure and accumulation of mercury. One conventional explanation for sex differences in mercury burden suggests female birds should have lower concentrations than conspecific males, because breeding females can depurate methylmercury to their eggs. However, sex differences in body burden of mercury among birds are not consistent. We used meta-analysis to synthesize 123 male-female comparisons of mercury burden from 50 studies. For breeding birds, males had higher concentrations of mercury than did females, supporting egg depuration as a mechanism. However, the percentage of female body mass represented by a clutch did not significantly predict the magnitude of the sex difference in mercury contamination, as predicted. Furthermore, whether species were semialtrical or altrical versus semiprecocial or precocial also did not explain sex differences in mercury burden. Foraging guild of a species did explain near significant variation in sex differences in mercury burden where piscivores and invertivores showed significant sex differences, but sex differences were not detected for carnivores, herbivores, insectivores, and omnivores. The magnitude and direction of sexual size dimorphism did not explain variation in sex differences in mercury burden among breeding birds. We reveal targeted research directions on mechanisms for sex differences in mercury and confirm that sex is important to consider for environmental risk assessments based on breeding birds.

[1]  D. Hoffman,et al.  Methylmercury chloride and selenomethionine interactions on health and reproduction in mallards , 1998 .

[2]  D. Spry,et al.  Toxicological significance of mercury in freshwater fish , 1996 .

[3]  W. Fleming Environmental metal residues in tissues of canvasbacks , 1981 .

[4]  Mark W. Lipsey,et al.  Practical Meta-Analysis , 2000 .

[5]  W. Braselton,et al.  Common loons (Gavia immer) nesting on low ph lakes in northern Wisconsin have elevated blood mercury content , 1995 .

[6]  Joanna Burger,et al.  Methodologies to examine the importance of host factors in bioavailability of metals. , 2003, Ecotoxicology and environmental safety.

[7]  J. Ackerman,et al.  Mercury bioaccumulation and risk to three waterbird foraging guilds is influenced by foraging ecology and breeding stage. , 2009, Environmental pollution.

[8]  Robert W. Furness,et al.  Birds as monitors of environmental change , 1993 .

[9]  S D Walter,et al.  Effect sizes can be calculated for studies reporting ranges for outcome variables in systematic reviews. , 2007, Journal of clinical epidemiology.

[10]  K. Gaines,et al.  Clapper rails as indicators of mercury and PCB bioavailability in a Georgia saltmarsh system , 2008, Ecotoxicology.

[11]  D. Evers,et al.  Mercury and other Contaminants in Common Loons Breeding in Atlantic Canada , 2005, Ecotoxicology.

[12]  S. Chipps,et al.  Hepatic Element Concentrations of Lesser Scaup (Aythya affinis) During Spring Migration in the Upper Midwest , 2011, Archives of Environmental Contamination and Toxicology.

[13]  R. Zamani-Ahmadmahmoodi,et al.  Cattle egret (Bubulcus ibis) and Little egret (Egretta garzetta) as monitors of mercury contamination in Shadegan Wetlands of south-western Iran , 2010, Environmental monitoring and assessment.

[14]  J. Burger,et al.  Methodologies for assessing exposure to metals: speciation, bioavailability of metals, and ecological host factors. , 2003, Ecotoxicology and environmental safety.

[15]  J. Ackerman,et al.  Mercury demethylation in waterbird livers: Dose–response thresholds and differences among species , 2009, Environmental toxicology and chemistry.

[16]  P. Becker Egg mercury levels decline with the laying sequence in charadriiformes , 1992, Bulletin of environmental contamination and toxicology.

[17]  R. Zamani-Ahmadmahmoodi,et al.  Mercury Pollution in Three Species of Waders from Shadegan Wetlands at the Head of the Persian Gulf , 2010, Bulletin of environmental contamination and toxicology.

[18]  J. Smits,et al.  Immune function, stress response, and body condition in arctic-breeding common eiders in relation to cadmium, mercury, and selenium concentrations. , 2002, Environmental research.

[19]  H. Barnes The Northern Limits of Balanus Balanoides (L). , 1957 .

[20]  L. Hedges Distribution Theory for Glass's Estimator of Effect size and Related Estimators , 1981 .

[21]  J. French,et al.  Dietary Toxicity and Tissue Accumulation of Methylmercury in American Kestrels , 2009, Archives of environmental contamination and toxicology.

[22]  D. E. Gaskin,et al.  Mercury levels in Bonaparte's gulls (Larus Philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada , 1987 .

[23]  R. Furness,et al.  Kinetics, dose--response, and excretion of methylmercury in free-living adult Cory's shearwaters. , 2001, Environmental science & technology.

[24]  S. Mabury,et al.  Persistent halogenated organic contaminants and mercury in northern fulmars (Fulmarus glacialis) from the Canadian Arctic. , 2010, Environmental pollution.

[25]  G. Allinson,et al.  Trace Metal Concentrations in the Little Penguin (Eudyptula minor) from Southern Victoria, Australia , 2007, Bulletin of environmental contamination and toxicology.

[26]  L. Hedges Estimation of effect size from a series of independent experiments. , 1982 .

[27]  D. Evers,et al.  Mercury exposure in breeding common loons (Gavia immer) in central Ontario, Canada , 1998 .

[28]  G. Heinz Methylmercury: Reproductive and behavioral effects on three generations of mallard ducks , 1979 .

[29]  G. Gabrielsen,et al.  Cadmium, zinc, copper, arsenic, selenium and mercury in seabirds from the Barents Sea: levels, inter-specific and geographical differences. , 2003, The Science of the total environment.

[30]  J. Burger,et al.  Methodologies, bioindicators, and biomarkers for assessing gender-related differences in wildlife exposed to environmental chemicals. , 2007, Environmental research.

[31]  C. A. Hui Metal and Trace Element Burdens in Two Shorebird Species at Two Sympatric Wintering Sites in Southern California , 1998, Environmental monitoring and assessment.

[32]  H. Wilson,et al.  Concentrations of metals and trace elements in blood of spectacled and king eiders in northern Alaska, USA , 2004, Environmental toxicology and chemistry.

[33]  S. N. Wiemeyer,et al.  Environmental contaminants in surrogates, foods, and feathers of California condors (Gymnogyps californianus) , 1986, Environmental monitoring and assessment.

[34]  R. Furness,et al.  Heavy metal concentrations in the tissues of seabirds from Gough Island, South Atlantic Ocean , 1988 .

[35]  H. Wolterbeek,et al.  Have high selenium concentrations in wading birds their origin in mercury? , 1994, The Science of the total environment.

[36]  W. Braselton,et al.  Geographic trend in mercury measured in common loon feathers and blood , 1998 .

[37]  Ingram Olkin,et al.  Stochastically dependent effect sizes. , 1994 .

[38]  A. Esmaili-Sari,et al.  A multispecies-monitoring study about bioaccumulation of mercury in Iranian birds (Khuzestan to Persian Gulf): Effect of taxonomic affiliation and trophic level. , 2009, Environmental research.

[39]  D. Krabbenhoft,et al.  Ecotoxicology of mercury , 2003 .

[40]  M. Lajeunesse 13. Recovering Missing or Partial Data from Studies: A Survey of Conversions and Imputations for Meta-analysis , 2013 .

[41]  J. Ackerman,et al.  Mercury concentrations and space use of pre-breeding American avocets and black-necked stilts in San Francisco Bay. , 2007, The Science of the total environment.

[42]  R. Poppenga,et al.  Patterns and Interpretation of Mercury Exposure in Freshwater Avian Communities in Northeastern North America , 2005, Ecotoxicology.

[43]  M. Conover,et al.  Selenium and mercury concentrations in California gulls breeding on the Great Salt Lake, Utah, USA , 2009, Environmental toxicology and chemistry.

[44]  J. Ackerman,et al.  Mercury concentrations in blood and feathers of prebreeding forster's terns in relation to space use of san francisco bay, california, usa, habitats , 2008, Environmental toxicology and chemistry.

[45]  J. Ackerman,et al.  Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA , 2008, Environmental toxicology and chemistry.

[46]  H. Satoh,et al.  Heavy metal contamination status of Japanese cranes (Grus japonensis) in east Hokkaido, Japan‐extensive mercury pollution , 2007, Environmental toxicology and chemistry.

[47]  J. Burger A framework and methods for incorporating gender-related issues in wildlife risk assessment: gender-related differences in metal levels and other contaminants as a case study. , 2007, Environmental research.

[48]  K. Hobson,et al.  Regional differences in collagen stable isotope and tissue trace element profiles in populations of long-tailed duck breeding in the Canadian Arctic. , 2005, The Science of the total environment.

[49]  R. W. Lowe,et al.  Selenium and heavy metals in San Francisco Bay diving ducks , 1986 .

[50]  A. García-Fernández,et al.  Concentrations of Cadmium, Mercury and Selenium in Blood, Liver and Kidney of Common Eider Ducks from the Canadian Arctic , 2001, Environmental monitoring and assessment.

[51]  J. Bouquegneau,et al.  Ecotoxicological and pathological studies of common guillemots Uria aalge beached on the Belgian coast during six successive wintering periods (1989-90 to 1994-95) , 1997 .

[52]  Marc J. Lajeunesse,et al.  On the meta-analysis of response ratios for studies with correlated and multi-group designs. , 2011 .

[53]  B. Braune,et al.  Sex-Related Levels of Selenium, Heavy Metals, and Organochlorine Compounds in American White Pelicans (Pelecanus erythrorhyncos) , 1999, Archives of environmental contamination and toxicology.

[54]  R. Furness,et al.  The chemical form of mercury stored in South Atlantic seabirds. , 1989, Environmental pollution.

[55]  J. Burger,et al.  Heavy metal concentrations in the liver of three duck species: influence of species and sex. , 1987, Environmental pollution.

[56]  G. Arnqvist,et al.  MetaWin: Statistical Software for Meta-Analysis with Resampling Tests. Version 1.Michael S. Rosenberg , Dean C. Adams , Jessica Gurevitch , 1998 .

[57]  J. Burger,et al.  Heavy metals in laughing gulls: Gender, age and tissue differences , 1996 .

[58]  Eun-Young Kim,et al.  Mercury levels and its chemical form in tissues and organs of seabirds , 1996 .

[59]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[60]  M. Forbes,et al.  Evidence for sex differences in mercury dynamics in double-crested cormorants. , 2011, Environmental science & technology.

[61]  V. Kuban,et al.  Total mercury and mercury species in birds and fish in an aquatic ecosystem in the Czech Republic. , 2007, Environmental pollution.

[62]  D. Hoffman,et al.  Mercury accumulation and loss in mallard eggs , 2004, Environmental toxicology and chemistry.

[63]  T. Bollinger,et al.  Trace Elements in King Eiders and Common Eiders in the Canadian Arctic , 2001, Archives of environmental contamination and toxicology.

[64]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[65]  B. Braune,et al.  Mercury and Selenium in Livers of Waterfowl Harvested in Northern Canada , 2006, Archives of Environmental Contamination and Toxicology.

[66]  M. Pokras,et al.  Liver mercury and methylmercury concentrations in new England common loons (Gavia immer) , 1998 .

[67]  M. Hughes Water content of the salt glands and other avian tissues. , 1974, Comparative biochemistry and physiology. A, Comparative physiology.

[68]  C. Henny,et al.  DDE, selenium, mercury, and white-faced IBIS reproduction at Carson Lake, Nevada , 1989 .

[69]  R. Furness,et al.  Mercury levels in eggs, tissues, and feathers of herring gulls Larus argentatus from the German Wadden Sea Coast. , 1993, Environmental pollution.

[70]  J. Takekawa,et al.  Relating Body Condition to Inorganic Contaminant Concentrations of Diving Ducks Wintering in Coastal California , 2002, Archives of environmental contamination and toxicology.

[71]  J. González‐Solís,et al.  Metals and selenium as bioindicators of geographic and trophic segregation in giant petrels Macronectes spp. , 2002 .

[72]  M. Murray,et al.  Effects of Environmental Methylmercury on the Health of Wild Birds, Mammals, and Fish , 2007, Ambio.

[73]  H. E. Braun,et al.  Residues of organochlorine insecticides, industrial chemicals, and mercury in eggs and in tissues taken from healthy and emaciated common loons, Ontario, Canada, 1968–1980 , 1983, Archives of environmental contamination and toxicology.

[74]  M. Hindell,et al.  Mercury and cadmium concentrations in the tissues of three species of southern albatrosses , 1999, Polar Biology.

[75]  B. Braune Comparison of total mercury levels in relation to diet and molt for nine species of marine birds , 1987 .

[76]  J. Grand,et al.  Concentrations of trace elements in eggs and blood of spectacled and common eiders on the Yukon‐Kuskokwim Delta, Alaska, USA , 2002, Environmental toxicology and chemistry.

[77]  A. Kambamanoli-Dimou,et al.  Transfer of methylmercury to hens' eggs after oral administration , 1991, Bulletin of environmental contamination and toxicology.

[78]  J. Croxall,et al.  Feather mercury levels in seabirds at South Georgia: influence of trophic position, sex and age , 2002 .

[79]  N. Burgess,et al.  Methylmercury exposure associated with reduced productivity in common loons , 2008, Ecotoxicology.

[80]  M. Finley,et al.  Survival and reproductive success of black ducks fed methyl mercury , 1978 .

[81]  E. Miller,et al.  Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest , 2010, Ecotoxicology.