Using Scat Detection Dogs to Monitor Environmental Contaminants in Sentinel Species and Freshwater Ecosystems
Many contaminants are introduced into freshwater ecosystems worldwide. Preliminary investigations that focus on apex predator/sentinel species like otter and mink can inform more targeted follow-up studies. The feces of these elusive animals can be collected non-invasively for analysis of contaminants and complimentary genetics. Conservation detection dogs were used to locate otter and mink feces along five rivers in Montana for analysis of heavy metals, anthropogenic organic contaminants (AOCs) including pharmaceuticals and personal care products (PPCPs), polybrominated (PBDE) flame retardants, and genetics. With highest find rates of 6 and 20 fecal matter finds per km for otter and mink, respectively, and detection of all three focal contaminants in some fecal samples, this proved an excellent application of dogs. Recommendations for follow-up investigations are also provided.
KeywordsDog Detection Monitoring Water quality Otter Mink Sentinel species Indicator species Contaminant Heavy metal Flame retardant PBDE Anthropogenic organic contaminant (AOC) Pharmaceutical Freshwater River quality DNA Genetics
Special thanks to Megan Parker, Director of Research for Working Dogs for Conservation, and to Pepin, for their contribution to the field survey component of this study. Much appreciation is extended to Kristy Pilgrim at the National Genomics Center for Wildlife and Fish Conservation in Missoula, Montana, for diligently performing the genetics analyses, enthusiastically sharing her knowledge and providing invaluable feedback to earlier versions of this chapter. Likewise, Heiko Langner, formerly in the Department of Geosciences at the University of Montana, is thanked for regularly lending his advice and expertise to the heavy metals component of this work. The creativity, hard work, and good humor of Matt Young, also at the Department of Geosciences (water sample processing), and of Thor Halldorson in the Department of Chemistry at the University of Manitoba (for his part in the PBDE sample analyses), is gratefully acknowledged. Thanks to Alan Ramsay, Marirose Kuhlman, and Ray Vinkey for giving their time to participate in the surveyor performance comparison trials.
The work described in this chapter was made possible through the generous support of the Kenney Brothers Foundation (Wick Fund), the Cinnabar Foundation (Montana’s Conservation Fund), the Arthur L. ‘Bud’ and Elaine V. Johnson Foundation, and the Animal Welfare Institute, via a Christine Stevens Wildlife Award. N. Richards and D. (Smith) Woollett extend their sincere thanks to these funders for their generosity and backing.
- Agency for Toxic Substances and Disease Registry (ATSDR). (2004). Polybrominated diphenyl ethers factsheet. US Department of Health and Human Services. Available at: https://www.atsdr.cdc.gov/tfacts68-pbde.pdf. Accessed 8 Jan 2018.
- Anderson, H. M., McCafferty, D. J., Saccheri, I. J., & McCluskie, A. E. (2006). Non-invasive genetic sampling of the Eurasian otter (Lutra lutra) using hairs. Hystrix Italian Journal of Mammalogy, 17, 65–77.Google Scholar
- Belansky, P. (Sprava Narodnych Parkov, Varin (Slovak Republic)) Juraskova, A., Kantikova, M. (Statny Veterinarny Ustav, Dolny Kubin (Slovak Republic)) Cadmium, mercury and lead contents in the otter excrements in the Studeny potok and Orava streams [Slovak Republic]. (1998). Slovenský veterinársky časopis.Google Scholar
- Ben-David, M., Bowyer, R. T., & Faro, J. B. (1996). Niche separation by mink and river otters: Coexistence in a marine environment. Oikos, 75, 41–48.Google Scholar
- Burkhardt, M. R., ReVello, R. C., Smith, S. G., & Zaugg, S. D. (2005). Pressurized liquid extraction using water/isopropanol coupled with solid-phase extraction cleanup for industrial and anthropogenic waste-indicator compounds in sediment. Analytica Chimica Acta, 534, 89–100. https://doi.org/10.1016/j.aca.2004.11.023.
- Center for Environmental Research and Children’s Health – CERCH. (2012). Flame retardants: Polybrominated diphenyl ethers – PBDEs. CERCH Factsheet.Google Scholar
- Chanin, P. (2003). Monitoring the Otter Lutra. Conserving Natura 2000 Rivers Monitoring Series No. 10, English Nature, Peterborough.Google Scholar
- Dallas, J. F., Coxon, K. E., Sykes, T., Chanin, P. R. F., Marshall, F., Carss, D. N., Bacon, P. J., Piertney, S. B., & Racey, P. A. (2003). Similar estimates of population genetic composition and sex ratio derived from carcasses and faeces of Eurasian otter Lutra lutra. Molecular Ecology, 12, 275–282.CrossRefGoogle Scholar
- Flaherty, C. (1996). Montana’s water: The good, the bad and the beautiful. Available at: www.montana.edu/cpa/news/wwwpb-archives/reso/water.html. Accessed 6 Apr 2017.
- Foresman, K. (2012). Mammals of Montana (2nd ed.). Missoula: Mountain Press Publishing Company.Google Scholar
- Gandhi, N., Gewurtz, S. B., Drouillard, K. G., Kolic, T., MacPherson, K., Reiner, E. J., & Bhavsar, S. P. (2017). Polybrominated diphenyl ethers (PBDEs) in Great Lakes fish: Levels, patterns, trends and implications for human exposure. Science of the Total Environment, 15, 907–916. https://doi.org/10.1016/j.scitotenv.2016.10.043. Epub 2016 Nov 16.CrossRefGoogle Scholar
- Godwin, B. L., Albeke, S. E., Bergman, H. L., Walters, A., & Ben-David, M. (2015). Density of river otters (Lontra canadensis) in relation to energy development in the Green River Basin, Wyoming. Science of the Total Environment, 532, 780–790. https://doi.org/10.1016/j.scitotenv.2015.06.058. Epub 2015 Jun 28.CrossRefGoogle Scholar
- Gupta, V., & Bakre, P. (2013). Heavy metals contamination in mammalian wildlife of Talchaper Blackbuck Sanctuary vs Dhavadoli Protected Area of western Rajasthan, India. International Journal of Scientific & Technology Research, 2, 86–91.Google Scholar
- Gutleb, A. C. (1994). Heavy metals, OCPs and PCBs in spraints of the otter from Slovenia. IUCN Otter Specialist Group Bulletin, 10, 31–34.Google Scholar
- Gutleb, A. C., Schenck, C., & Staib, E. (1997). Giant otter (Pteronura brasiliensis) at risk? Total mercury and methyl mercury levels in fish and otter scats, Peru. Ambio, 26, 511–514.Google Scholar
- Hale, R. C., La Guardia, M. J., Harvey, E., Chen, D., Mainor, T. M., Luellen, D. R., & Hundal, L. S. (2012). Polybrominated diphenyl ethers in U.S. sewage sludges and biosolids: Temporal and geographical trends and uptake by corn following land application. Environmental Science & Technology, 46, 2055–2063. https://doi.org/10.1021/es203149g. Epub 2012 Feb.CrossRefGoogle Scholar
- Han, S. Y., Son, S. W., Ando, M., & Sasaki, H. (1998). Heavy metals and PCBs in Eurasian otters (Lutra lutra) in South Korea. Proceedings of the VIIth International Otter Colloquium, 103–109. Available at: http://www.otterspecialistgroup.org/Bulletin/Volume19A/Trebon-II.pdf. Accessed 8 Jan 2018.
- Henny, C.J., and Elliott, J.E. (2007). Chapter 18: Toxicology. In D.M. Bird, & K. L. Bildstein, Eds., Raptor Research and Management Techniques (pp. 329–350). Washington, DC: Raptor Research Foundation.Google Scholar
- Jansman, H., Chanin, P., & Dallas, J. F. (2001). Monitoring otter populations by DNA typing of spraints. IUCN Otter Specialist Group Bulletin, 18, 11–16.Google Scholar
- Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Pääbo, S., Villablanca, F. X., & Wilson, A. C. (1989). Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the Natural Academy of Science, USA, 86, 6196–6200.CrossRefGoogle Scholar
- Koelewijn, H. P., Perez-Haro, M., Jansman, H., Boerwinkel, M. C., Bovenschen, J., Lammertsma, D. R., Niewold, F. J., & Kuiters, A. T. (2010). The reintroduction of the Eurasian otter (Lutra lutra) into the Netherlands: Hidden life revealed by non-invasive genetic monitoring. Conservation Genetics, 11, 601–614.CrossRefGoogle Scholar
- Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., & Buxton, H. T. (2002). Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: A national reconnaissance. Environmental Science & Technology, 36, 1202–1211.CrossRefGoogle Scholar
- Letcher, R. J., Lu, Z., Chu, S., Haffner, G. D., Drouillard, K., Marvin, H. C., & Ciborowski, J. H. (2015). Hexabromocyclododecane flame retardant isomers in sediments from Detroit River and Lake Erie of the Laurentian Great Lakes of North America. Bulletin of Environmental Contamination and Toxicology, 95, 31–36.CrossRefGoogle Scholar
- MacKay, P., Smith, D. A., Long, R. A., & Parker, M. (2008). In R. A. Long, P. Mackay, W. Zielinski, & J. Ray (Eds.), Chapter 7: Noninvasive survey methods for carnivores. Scat detection dogs (pp. 183–222). Washington, DC: Island Press.Google Scholar
- Melquist, W. E., & Dronkert, A. E. (1987). River otter. In M. Novak, J. A. Baker, M. E. Obbard, & B. Malloch (Eds.), Wild furbearer management and conservation in North America (pp. 625–641). North Bay: Ontario Trappers Association.Google Scholar
- Montana Department of Environmental Quality (MDEQ). (n.d.). Yellowstone River district. Available at: http://deq.mt.gov/Land/AbandonedMines/linkdocs/193tech. Accessed 8 Jan 2018.
- Moraes, L. M. B., Ferreira, C. L., Adriano, L. R., Silva, R. M. C., Nascimento Filho, V. F., & Ferreira, J. R. (2005). Use of X-ray fluorescence energy dispersive technique in the lead determination and other metals in excrements of otters (Lontra longicaudis). Associacao Brasileira de Energia Nuclear, Rio de Janeiro, RJ (Brazil); [4886 p.]; ISBN 85-99141-01-5; Worldcat; 2005; [6 p.]; INAC 2005: International nuclear Atlantic conference. Nuclear energy reducing global warming; 14. Brazilian national meeting on reactor physics and thermal hydraulics; 7. Brazilian national meeting on nuclear applications; Santos, SP (Brazil).Google Scholar
- National Park Service (NPS). (2017, November 17). Timeline of human history in Yellowstone. Available at: www.nps.gov/yell/learn/historyculture/timeline.htm. Accessed 8 Jan 2018.
- Newton, D. E. (2012). Northern River Otter population assessment and connectivity in Western Montana. MSc. Thesis. Paper 4186. Available at: http://scholarworks.umt.edu/etd/4186. Accessed 7 Jan 2018.
- O’Neill, D., Turner, P. D., O’Meara, D. B., Chadwick, E. A., Coffey, L., & O’Reilly, C. (2013). Development of novel real-time TaqMan(®) PCR assays for the species and sex identification of otter (Lutra lutra) and their application to noninvasive genetic monitoring. Molecular Ecology Resources, 13, 877–883. https://doi.org/10.1111/1755-0998.12141.
- Pierson, J., Luikart, G., & Schwartz, M. (2015). Chapter 15: The application of genetic indicators in wild populations: Potential and pitfalls for genetic monitoring. In D. B. Lindenmaye, J. C. Pierson, & P. Barton (Eds.), Indicators and surrogates of biodiversity and environmental change (pp. 149–159). Boca Raton: CRC Press, CSIRO Press.Google Scholar
- Pountney, A., Stevens, J. R., Sykes T., & Tyler, C. (2009). Population genetics and PBDE analysis of English and Welsh otters. Environment Agency Report No. SC040024/SR1. Available at: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/291009/scho0909bqzc-e-e.pdf. Accessed 8 June 2017.
- Pycke, B. F. C., Roll, I. B., Brownawell, B. J., Kinney, C. A., Furlong, E. T., Kolpin, D. W., & Halden, R. U. (2014). Transformation products and human metabolites of triclocarban and triclosan in sewage sludge across the United States. Environmental Science and Technology, 48, 7881–7890.CrossRefGoogle Scholar
- Ramos-Rosas, N. N., Valdespino, C., García-Hernández, J., Gallo-Reynoso, J. P., & Olguín, E. J. (2013). Heavy metals in the habitat and throughout the food chain of the Neotropical otter, Lontra longicaudis, in protected Mexican wetlands. Environmental Monitoring and Assessment, 85, 1163–1173.Google Scholar
- Richards, N. L., Hall, S. W., Harrison, N. M., Gautam, L., Scott, K. S., Dowling, G., Zorilla, I., & Fajardo, I. (2014). Merging wildlife and environmental monitoring approaches with forensic principles: Application of unconventional and non-invasive sampling in eco-pharmacovigilance. Journal of Forensic Research. Available at: https://www.omicsonline.org/open-access/merging-wildlife-and-environmental-monitoring-approaches-with-forensic-principles-application-of-unconventional-and-noninvasive-sampling-in-eco-pharmacovigilance-2157-7145.1000228.php?aid=26623. Accessed 8 Jan 2018.
- Sonne, C., Leifsson, P. S., Dietz, R., Born, E. W., Letcher, R. J., Hyldstrup, L., Riget, F. F., Kirkegaard, M., & Muir, D. C. (2006). Xenoendocrin pollutants may reduce size of sexual organs in east Greenland polar bears (Ursus maritimus). Environmental Science & Technology, 40, 5668–5674.CrossRefGoogle Scholar
- Taggart, M., Richards, N. L., & Kinney, C. (2015). Impacts of pharmaceuticals on the terrestrial environment. In R. Hester (Ed), Pharmaceuticals in the environment. Issues in Environmental Science & Technology (pp. 216–254). Cambridge: Royal Society of Chemistry.Google Scholar
- US Department of Agriculture (USDA), Forest Service, Fire and Aviation Management. (2015). Implementation guide for aerial application of fire retardant. Fire and Aviation Management, Washington, DC. Available at: https://www.fs.fed.us/fire/retardant/afr_handbook.pdf. Accessed 8 Jan 2018.
- Woollett, D., Hurt, A., & Richards, N. L. (2014). The current and future role of free-ranging detection dogs. In M. Gompper (Ed.), Free-ranging dogs and wildlife conservation (pp. 239–264). Oxford: Oxford University Press. https://doi.org/10.1093/acprof:osobl/9780199663217.003.0010.CrossRefGoogle Scholar
- Zhang, S., Bursian, S., Martin, P. A., Chan, H. M., & Martin, J. W. (2008). Dietary accumulation, disposition, and metabolism of technical pentabrominated diphenyl ether (de-71) in pregnant mink (Mustela vison) and their offspring. Environmental Toxicology & Chemistry, 27, 1184–1193. https://doi.org/10.1897/07-487.1.CrossRefGoogle Scholar