Effects of halogenated contaminants on reproductive development in wild mink (Neovison vison) from locations in Canada
The concept of the Anthropocene, that humans are now re-engineering global ecosystems, is in part evidenced by the pervasive pollution by persistent organic pollutants (POPs). Certain POPs are hormone mimics and can disrupt endocrine and hence reproductive processes, shown mainly by laboratory studies with model species. There are, in contrast, fewer confirmations of such disruption from eco-epidemiological studies of wild mammals. Here we used the American mink (Neovison vison) as a sentinel species for such a study. Over the period 1998–2006, 161 mink carcasses were obtained from commercial trappers in the Canadian provinces of British Columbia and Ontario. Mink were aged, sexed, measured, and body condition assessed. Livers were analyzed either individually or pooled for organochlorine (OC) pesticides, polychlorinated biphenyls (PCBs), and subsets for polybrominated diphenyl ethers (PBDEs). We primarily addressed whether contaminants affected male reproductive development by measuring baculum size and assessing the influences of age and body condition. We also considered the influence of spatial variation on relative exposure and size of baculum. Statistical models separated by age class revealed that significant relationships between baculum length or mass and juvenile mink were mostly positive, whereas for adults and first year mink they were mostly negative. A significant negative relationship for adult mink was determined between DDE and both baculum length and mass. For juvenile mink we found significant positive relationships between ∑PCBs, DDE and ∑PBDEs with baculum length. Our results provide some indication of negative effects of halogenated contaminants on male reproductive development in wild mink, and the most likely candidate chemical is the confirmed anti-androgenic compound, DDE, rather than PCBs or other compounds.
KeywordsMink Neovison vison Reproduction Baculum POPs DDE Endocrine disruption
We thank the many trappers throughout the provinces of British Columbia and Ontario for providing carcasses. Dr. M. McAdie, H. Gill, M. Fronteddu for tissue collection, cleaning and measurements; G. Savard coordinated the tissue preparation of liver samples for chemistry. H. Won, P. Dunlop, B. Wakeford, K. Drouillard and N. Ismali are thanked for their work on the chemical analyses. B. Hunter provided advice on veterinary pathology. M. Anderson provided R statistical advice for multivariate modelling in PERMANOVA+, and R. Brook who assisted with GLMM models.
Funding was provided mainly by the Georgia Basin and Great Lakes Action Plans of Environment and Climate Change Canada to J. Elliott and P. Martin, respectively.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
The animals used in this study were obtained solely from trappers licensed under the governments of British Columbia and Ontario, and the principle investigators had the required carcass possession permits from those governments.
- Anderson MJ, Clarke KR, Gorley RN (2008) PERMANOVA+ for Primer vs. 6: User Manual/tutorial. Primer-E, Plymouth, UKGoogle Scholar
- Birks JD, Linn IJ (1982) Studies of home range of the feral mink, Mustela vison. Proc Zool Soc Lond 49:231–257Google Scholar
- Bleavins MR, Aulerich RJ, Ringer RK (1982) Placental and mammary transfer of polychlorinated and polybrominated biphenyls in the mink and ferret. ASTM STP 757:121–131Google Scholar
- Bursian SJ, Sharma C, Aulerich RJ, Yamini B, Mitchell RR, Orazio CE, Moore DR, Svirsky S, Tillitt DE (2006) Dietary exposure of mink (Mustela vison) to fish from the Housatonic River, Berkshire County, Massachusetts, USA: effects on reproduction, kit growth, and survival. Environ Toxicol Chem 25(6):1533–1540CrossRefGoogle Scholar
- Clarke KR, Gorley RN (2014) Primerv7: User manual/tutorial. Primer-E, PlymouthGoogle Scholar
- Grove RA (2006) Environmental contaminants in male river otters collected from Oregon and Washington, 1994-99, with reproductive organ hypoplasia observed in otter males. PhD Dissertation, Oregon State UniversityGoogle Scholar
- Guillette LJ, Crain DA, Gunderson MP, Kools SAE, Milnes MR, Orlando EF, Rooney AA, Woodward AR (2000) Alligators and endocrine disrupting contaminants: a current perspective. Am Zool 40(3):438–452Google Scholar
- Harris ML, Wilson LK, Norstrom RJ, Elliott JE (2003b) Egg concentrations of polychlorinated dibenzo-p-dioxins and dibenzofurans in double-crested (Phalacrocorax auritus) and Pelagic (P. pelagicus) cormorants from the Strait of Georgia, Canada, 1973− 1998. Environ Sci Technol 37:822–831CrossRefGoogle Scholar
- Haynes JM, Wellman ST, Beckett KJ, Pagano JJ, Fitzgerald SD, Bursian SJ (2009) Histological lesions in mink jaws are a highly sensitive biomarker of effect after exposure to TCDD-like chemicals: field and literature-based confirmations. Arch Environ Contam Toxicol 57(4):803–807CrossRefGoogle Scholar
- Henny CJ, Blus LJ, Gregory SV, Stafford CJ (1981) PCBs and organochlorine pesticides in wild mink and river otters from Oregon. In: Worldwide Furbearer Conference Proceedings. Patuxent Wildlife Research Center, Frostburg, Maryland, pp 1763–1780Google Scholar
- Hochstein Jr MS, Render JA, Bursian SJ, Aulerich RJ (2001) Chronic toxicity of dietary 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Vet Hum Tox 43:134–139Google Scholar
- Huang AC, Nelson C, Elliott JE, Guertin D, Ritland C, Douillard K, Cheng KM, Schwantje HM (2018) River Otters (Lontra canadensis) “trapped” in a coastal environment contaminated with persistent organic pollutants: demographic and physiological consequences. Environ Pollut 238:306–316. (in press)Google Scholar
- Kean EF, Lyons G, Chadwick EA (2013) Persistent organic pollutants and indicators of otter health. A CHEM Trust Report. Cardiff University. UK. www.chemtrust.org.uk
- Martin PA, McDaniel TV, Huges KD, Hunter B (2017) Organochlorine contaminants in wild mink from the lower Great Lakes Basin, Canada, 1998-2006. Environ Monit Assess 189:459–471. (in press)Google Scholar
- Matson GM (1981) Workbook for Cementum analysis. Matson’s Laboratory, Milltown, Montana, USAGoogle Scholar
- Miller AA, Elliott JE, Elliott KH, Guigueno MF, Wilson LK, Lee S, Idrissi A (2014) Spatial and Temporal trends in Brominated Flame Retardants in Seabirds from the Pacific Coast of Canada. Environ Pollut. 195:48-55. http://dx.doi.org/10.1016/j.envpol.2014.08.009
- Paul JR (1968) Baculum development in mink. Trans Ill State Acad Sci 61:308–309Google Scholar
- SAS Instit (2000) SAS/STAT Users Guide: Statistics. Release 8. SAS Institute, Cary, North CarolinaGoogle Scholar
- You L, Casanova M, Archibeque-Engle S, Sar M, Fan LQ, Heck HD (1998) Impaired male sexual development in perinatal Sprague–Dawley and Long–Evans Hooded Rats exposed in utero and lactationally to, p′-DDE. Toxicol Sci 45:162–173Google Scholar
- Wong LIL, Labrecque M, Ibuki N, Cox ME, Elliott JE, Beischlag TV (2015) P,p′-Dichlorodiphenyltrichloroethane (p,p′-DDT) and p,p′-dichlorodiphenyldichloroethylene (p,p′-DDE) repress prostate specific antigen levels in human prostate cancer cell lines. Chem Biol Interact 230:40–49CrossRefGoogle Scholar
- Zhang S, Bursian SJ, Martin PA, Chan HM, Tomy G, Palace VP, Mayne GJ, Martin JW (2009) Reproductive and developmental toxicity of a pentabrominated diphenyl ether mixture, DE-71, to ranch mink (Mustela vison) and hazard assessment for wild mink in the Great Lakes region. Toxicol Sci 110:107–116CrossRefGoogle Scholar
- Zwiernik MJ, Kay DP, Moore J, Beckett KJ, Seong Khim J, Newsted JL, Roark SA, Giesy JP (2008) Exposure and effects assessment of resident mink (Mustela vison) exposed to polychlorinated dibenzofurans and other dioxin-like compounds in the Tittabawassee River Basin, Midland, Michigan, USA. Environ Toxicol Chem 27(10):2076–2087CrossRefGoogle Scholar