Climate-induced behavioral changes influence exposure of polar bears to pathogens and contaminants

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Climate-induced behavioral changes influence exposure of polar bears to pathogens and contaminants T. Atwood 1, C. Duncan 2, K. Patyk 3, P. Nol 4, J. Rhyan 4, M. McCollum 4, M. McKinney 5, A. Ramey 1, O. Kwok 6, C. Cerqueira-Cézar 6, J. Dubey 6, and S. Hennager 7 1 USGS Alaska Science Center, 2 Colorado State University, 3 USDA-Veterinary Services-CEAH, 4 USDA- National Wildlife Research Center, 5 University of Connecticut, 6 USDA- Agricultural Research Service, 7 USDA- National Veterinary Services Laboratories

Outline Background - why do we care? Environmental changes in the Beaufort - influence on bear behavior Methods, results, discussion

Why do we care about polar bear health? Disease and Predation was a listing factor considered in the ESA determination there is a need to monitor health and identify early changes that may negatively impact subpopulations

U.S. Conservation Management Plan:

Ecosystem sentinels

Food safety insight

A Changing Arctic Marine Ecosystem

Over the last 4 decades Extent: -14.2%/decade - in AK, -12%/decade

Large areas of summer sea ice habitat gone

Proportion Mean # of days on shore (Aug-Oct) A growing percentage coming ashore in summer 0.40 25% 0.30 0.20 4% 0.10 r = 0.77 0.00 1985 1990 1995 2000 2005 2010 2015 Year 100 90 80 70 60 50 40 30 20 10 0 r = 0.64 0 20 40 60 80 100 120 Duration (days) of the open water season Atwood et al. 2016. PLoS ONE.

McKinney et al. 2017. Ecosphere.

Have environmentally-driven behavioral changes altered patterns of exposure to pathogens and contaminants?

Methods Pathogens (serum: 2007-14) - Brucella spp., T. gondii: marine and terrestrial - F. tularensis, N. caninum: terrestrial - C. burnetii: emerging Contaminants (plasma: 2012-14) - ΣPCB, ΣClBz, ΣHCH, ΣCHL, and ΣDDT

Lab Pathogen Test Titer Cut-Off Lab Brucella card test/standard plate test C. burnetii indirect fluorescence assay T. gondii modified agglutination test N. caninum Neospora agglutination test F. tularensis commercial slide agglutination test NA NVSL 1:128 CSU 1:25 APDL 1:25 APDL 1:20 ASC

Analysis Estimated observed seroprevalence - epir Characterized risk factors - GLMMs (pathogens) - ANOVAs (contaminants)

Observed seroprevalence: 2007-14 C. burnetii* T. gondii Brucella spp. F. tularensis* N. caninum* seropositive (n) 38 33 18 5 5 seronegative (n) 100 105 120 103 133 mean seroprevalence 27.6% 23.9% 13.0% 4.8% 3.7% 95% CI 20.4 35.7 17.1 31.2 8.1 19.7 1.9 10.8 1.2 7.3 *1 st detections in polar bears and Arctic marine mammals

Co-infection? Evidence for prior exposure to >1 pathogen was rare Evidence of Co-Occurrence Seroprevalence C. burnetii x T. gondii 2.9% C. burnetii x Brucella 2.2% T. gondii x N. caninum 1.5% Brucella x T. gondii 1.4% Brucella x F. tularensis 0.9% F. tularensis x N. caninum 0.9%

Observed seroprevalence Apparent prevalence of T. gondii and Brucella over time 35 T. gondii Brucella spp. 30 25 20 15 10 5 0 early 1990s early 2000s 2007-14 Assessment period

Seroprevalence Risk factors for exposure to pathogens land-based bears ice-based bears 0.5 0.4 *P<0.001 0.3 0.2 *P=0.01 0.1 0 C. burnetii T. gondii Brucella F. tularensis N. caninum Pathogen

ng/g in blood Contaminant concentrations 40 2003 2007-14 -55% 20 +30% 0 ΣPCB ΣClBz ΣHCH ΣCHL ΣDDT Contaminant

ng/g in blood Risk factors for exposure to contaminants 16 land ice -15% P=0.56-22% P=0.05 12 8 4 0 ΣPCB ΣClBz ΣHCH ΣCHL ΣDDT Contaminant

Key findings Likely increase in seroprevalence Brucella and T. gondii 1 st evidence of exposures to Coxiella, Francisella, Neospora Evidence that climate-induced change in behavior may be influencing some exposures

Why increasing pathogen exposures? Evidence suggests T. gondii has become more prevalent Brucella recognized as infecting both terrestrial and marine spp. Coxiella, Francisella, Neospora: northward expansion? - Francisella and Neospora only detected in land-based bears

And, why declining contaminant exposures? PCBs and CHLs are highly bio-magnifying Concentrations influenced by trophic position of prey lower THg concentrations associated with lower proportions of ringed seal consumed and greater proportions of bowhead whale consumed. McKinney et al. 2017

Management implications Consequences of exposures largely unknown - Cox/Bruc/Neo associated with reproductive pathology - T. gondii linked to compromised immune function Trend of land use likely to increase - costs of increased pathogen exposures likely to outweigh benefits of reduced contaminant concentrations

Acknowledgments Field: G. Durner, K. Simac, A. Pagano, S. Winterrowd, K. Rode, L. Peacock, T. Donnelly, S. Amstrup, G. York Aerial support: Prism Helicopters, Soloy Helicopters, Maritime Helicopters Primary funding: North Pacific Research Board USGS- Changing Arctic Ecosystems

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