Marsh Wrens As Bioindicators of Mercury in Wetlands of Great Salt Lake

May 6, 2013 - Nonlethal sampling of bird blood and feathers are among the more common ways of estimating the risk of mercury exposure to songbird repr...
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MARSH WRENS AS BIOINDICATORS OF MERCURY IN WETLANDS OF GREAT SALT LAKE: DO BLOOD AND FEATHERS REFLECT SITE-SPECIFIC EXPOSURE RISK TO BIRD REPRODUCTION? Christopher Alex Hartman, Josh T Ackerman, Garth Herring, John Isanhart, and Mark Herzog Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es400910x • Publication Date (Web): 06 May 2013 Downloaded from http://pubs.acs.org on May 13, 2013

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MARSH WRENS AS BIOINDICATORS OF MERCURY IN WETLANDS OF GREAT SALT LAKE: DO BLOOD AND FEATHERS REFLECT SITE-SPECIFIC EXPOSURE RISK TO BIRD REPRODUCTION?

C. Alex Hartman1, *, Joshua T. Ackerman1, Garth Herring1, John Isanhart2, and Mark Herzog1 1

U. S. Geological Survey, Western Ecological Research Center, Dixon Field Station, 800 Business Park Drive, Suite D, CA 95620, USA 2

U.S. Fish and Wildlife Service, Salt Lake City, UT 84119, USA

ABSTRACT. Non-lethal sampling of bird blood and feathers are among the more common ways of estimating the risk of mercury exposure to songbird reproduction. The implicit assumption is that mercury concentrations in blood or feathers of individuals captured in a given area are correlated with mercury concentrations in eggs from the same area. Yet, this assumption is rarely tested. We evaluated mercury concentrations in blood, feathers, and eggs of marsh wrens in wetlands of Great Salt Lake, Utah, and, at two spatial scales, specifically tested the assumption that mercury concentrations in blood and feather samples from birds captured in a defined area were predictive of mercury concentrations in eggs collected in the same area. Mercury concentrations in blood were not correlated with mercury concentrations in eggs collected within the same wetland unit, and poorly correlated with mercury concentrations in eggs collected at the smaller home range spatial scale of analysis. Moreover, mercury exposure risk, as estimated via tissue concentrations, differed among wetland units depending upon whether blood or egg mercury concentrations were sampled. Mercury concentrations in feathers also were uncorrelated with mercury concentrations in eggs, and poorly correlated with mercury concentrations in blood. These results demonstrate the potential for contrasting management actions that may be implemented based solely on the specific avian tissue that is sampled, and highlights the importance of developing avian tissues as biomonitoring tools for assessing local risk of mercury exposure to bird reproduction.

* Corresponding author: [email protected]; phone: 530-669-5085

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INTRODUCTION Mercury is a global pollutant that is highly toxic to wildlife, adversely impacting behavior, survival, and reproduction.1 Continued mercury deposition over time has led to increased efforts and expanded monitoring programs to assess exposure risk to wildlife.2,3 Piscivorous waterbirds are frequently used as bioindicators of mercury exposure because they occupy a high trophic level and thus are subject to mercury biomagnification,4,5 and because legacy mercury pollution can cause aquatic ecosystems to have elevated levels of mercury exposure.6,7 More recently, insectivorous songbirds have been used to monitor mercury exposure within aquatic and terrestrial food webs8,9 and some studies have found evidence of reduced reproductive success associated with elevated tissue mercury levels.10 Insectivorous songbirds are widespread and abundant, occupy both aquatic and terrestrial habitats, have small feeding territories,11 and often can be sampled easily − all attributes that make songbirds potentially useful as spatially precise bioindicators of mercury exposure to wildlife. However, as with all potential bioindicators, correct interpretation of results requires an understanding of the species ecology, and how mercury concentrations in different tissues translate to exposure risk. In particular, it is necessary to select appropriate tissues when using songbirds as bioindicators of mercury exposure. Whole eggs are an ideal tissue for evaluating the risk of mercury exposure in birds because reproduction is among the most sensitive endpoints for mercury toxicity in birds,1 eggs have among the best developed toxicity thresholds,12 and eggs typically represent mercury exposure from a discrete time period during breeding.13 Therefore, egg mercury concentrations often are the most direct approximation of mercury risk to reproduction in birds. Yet, non-lethal sampling of bird blood and feathers are among the more popular methods for approximating songbird mercury exposure in the environment.14,15 The implicit assumption, however, is that mercury concentrations in blood and feathers are reliable indices of the potential risk of mercury to bird reproduction in the sampled area. Previous studies have found strong positive correlations between a female’s blood mercury concentration and

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3 mercury concentration in eggs from her clutch,16,17 but see 18 However, the assumption that mercury concentrations in blood samples of birds captured in a specific area are correlated with mercury concentrations of eggs collected from the same area is rarely tested. Because maternal blood mercury concentrations are correlated with egg mercury concentrations, it often is assumed that mercury concentrations of blood sampled from birds captured in a given area will be reflective of egg mercury concentrations in that same area. Yet, there are several reasons why this might not occur, including bird movements, diet, timing of sampling, sampling of transient individuals, and dynamics of mercury depuration into eggs. In this paper, we assessed the strength of correlations in mercury concentrations among blood, feathers, and eggs of marsh wrens (Cistothorus palustris) breeding in wetlands of Great Salt Lake. In particular, we tested the assumption that blood and feather mercury concentrations of individuals captured in a defined area are reflective of mercury concentrations in eggs collected from the same area. We tested whether mercury concentrations in blood and feathers were correlated with mercury concentrations in eggs at two spatial scales: (1) within the same wetland unit (the scale at which conservation and management actions often occurs), and (2) within a smaller area more closely representative of a marsh wren’s home range (a scale which relates directly to the species’ ecology). We also evaluated individualbased correlations in mercury concentrations among blood and feather samples, and illustrate how the strength of these correlations varies among wetland units and age-sex classes. Our results highlight the potential pitfalls of using proxy tissue matrices, such as bird blood or feathers, without first developing these tissues as suitable biomonitoring tools to infer local risk of mercury exposure to bird reproduction.

MATERIALS AND METHODS Study area and sample collections We studied mercury concentrations in marsh wrens at the Bear River Migratory Bird Refuge (BRMBR), Great Salt Lake, Utah (41.47° N, 112.26° W) in June and July of 2011 (see Supporting Information for study site and species details). We focused on marsh wrens in this study because they have small

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4 territories (60-10,000 m2), are widespread and abundant,19 and recent studies have suggested that songbirds in general12 and wrens in particular,10 may be vulnerable to mercury contamination. We captured marsh wrens using mist nets (12 m long, 30 mm mesh) at 12 sites within eight wetland units of the BRMBR. We selected capture sites based on the presence of marsh wrens and active marsh wren nests, but also on proximity to the Bear River and Great Salt Lake. Five sites in four wetland units were located in the region where the Bear River first empties into the refuge complex, and seven sites in four wetland units were located several kilometers away towards the Great Salt Lake, thereby allowing for a potential contrast in mercury concentrations between tissues collected at the Bear River inflow into the BRMBR and outflow from the BRMBR into the Great Salt Lake. Capture sites, both within and across wetland units, were separated by a minimum of 250 m, and most capture sites were separated by more than 500 m. At each capture site, we erected 1-2 mist nets and broadcast a recording of marsh wren calls and song using a portable audio player and 3-watt speaker system. Universal Transverse Mercator (UTM) coordinates were recorded at the midpoint of each mist net using a handheld GPS unit (position accuracy < 5 m). Each captured bird was banded with a U.S. Geological Survey metal band. We used plumage to assign birds to one of two age classes following Pyle20: (1) after-hatch-year adults (individuals that hatched in a previous year), and (2) hatch-year juveniles (individuals that hatched in the current year). We identified adult birds’ sex, using the degree of cloacal protuberance for males and the presence of a brood patch for females,20 and we confirmed sex using genetic analysis (Zoogen Services, Davis, California, USA) for all but two individuals. Unlike eastern marsh wrens, western marsh wrens are thought to undergo a single prebasic molt after the breeding season.21 However, a few specimens collected in California in the spring were found to be molting some feather tracts.21 We therefore sampled multiple feather tracts to account for differences in feather mercury concentrations associated with potential differences in the timing of feather molt among feather tracts. We collected back, breast, and head feathers (approximately 12-15 individual feathers from each feather tract) from each captured bird and stored them in Whirl-paks® (Nasco, Modesto, California, USA) until laboratory analysis. Back feathers collected were restricted to the distinct black triangular patch with white streaks on the upper

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5 back. We collected whole blood from each marsh wren from the jugular vein using a heparinized 26 gauge needle and syringe. Blood volume collected was restricted to ≤1% body mass (