Mercury Contamination within Terrestrial Ecosystems in New England ...

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Jan 27, 2012 - Albany, NY 12205 ... SUGGESTED CITATION: Osborne, C. E, D. C. Evers, M. Duron, N. Schoch, D. Yates, D. Buck, O. P.. Lane, and J. Franklin.
Mercury Contamination within Terrestrial Ecosystems in New England and Mid-Atlantic States: Profiles of Soil, Invertebrates, Songbirds, and Bats

Mercury Contamination within Terrestrial Ecosystems in New England and Mid-Atlantic States: Profiles of Soil, Invertebrates, Songbirds, and Bats

SUBMITTED TO: Dr. Tim Tear The Nature Conservancy – Eastern New York Chapter 195 New Karner Road Albany, NY 12205 SUBMITTED BY: Biodiversity Research Institute 652 Main St. Gorham, Maine, USA 04038 (207-839-7600) FINAL DRAFT SUBMITTED ON: 27 January 2012 Biodiversity Research Institute

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Biodiversity Research Institute (BRI) is a 501(c)3 nonprofit organization located in Gorham, Maine. The mission of Biodiversity Research Institute is to assess ecological health through collaborative research, and to use scientific findings to advance environmental awareness and inform decision makers. To obtain copies of this report contact: Biodiversity Research Institute 19 Flaggy Meadow Road Gorham, ME 04038 (207) 839-7600 www.briloon.org

COVER ILLUSTRATION: Shearon Murphy SUGGESTED CITATION: Osborne, C. E, D. C. Evers, M. Duron, N. Schoch, D. Yates, D. Buck, O. P.

Lane, and J. Franklin. 2011. Mercury Contamination within Terrestrial Ecosystems in New England and Mid-Atlantic States: Profiles of Soil, Invertebrates, Songbirds, and Bats. Report BRI 2011-09. Submitted to The Nature Conservancy – Eastern New York Chapter. Biodiversity Research Institute, Gorham, Maine. Biodiversity Research Institute

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Table of Contents LIST OF FIGURES ................................................................................................................................................... 5 LIST OF TABLES..................................................................................................................................................... 9 1.0 EXECUTIVE SUMMARY ............................................................................................................................. 10 2.0 INTRODUCTION .......................................................................................................................................... 11 3.0 SOILS ................................................................................................................................................................ 15 3.1 STUDY AREA .................................................................................................................................. 15 3.2 METHODS ....................................................................................................................................... 15 3.3 RESULTS AND DISCUSSION ..................................................................................................... 16 3.3.1 MERCURY LEVELS IN SOIL ............................................................................................ 16 3.3.2.1 SOIL MOISTURE .............................................................................................................. 17 3.3.2.2 SOIL CHEMISTRY ........................................................................................................... 18 3.4 CONCLUSION ................................................................................................................................. 21 4.0 INVERTEBRATES ........................................................................................................................................ 22 4.1 STUDY AREA ................................................................................................................................... 22 4.2 METHODS ........................................................................................................................................ 22 4.2.1 STATISTICAL ANALYSIS ................................................................................................. 23 4.3 RESULTS AND DISCUSSION ...................................................................................................... 23 4.3.1 SAMPLING EFFORT ........................................................................................................... 23 4.3.2. REGIONAL AND SPECIES MERCURY EXPOSURE.................................................. 23 4.4 CONCLUSION .................................................................................................................................. 28 5.0 SONGBIRDS ................................................................................................................................................... 29 5.1 STUDY AREA .................................................................................................................................... 29 5.2 METHODS ......................................................................................................................................... 29 5.2.1 STATISTICAL ANALYSIS ................................................................................................. 29 5.3 RESULTS AND DISCUSSION ........................................................................................................ 31 5.3.1 SAMPLING EFFORT ........................................................................................................... 31 5.3.2 REGIONAL AND SPECIES MERCURY EXPOSURE .................................................. 31 5.3.2.1 CASE STUDY #3 - SALTMARSH SPARROW .......................................................... 34 5.3.2.2 CASE STUDY #4 - RUSTY BLACKBIRD ................................................................... 35 5.3.3 MERCURY EXPOSURE BY FORAGING GUILD .......................................................... 37 5.3.3.1 CASE STUDY # 5 - RELATIONSHIP BETWEEN SOIL Hg AND A GROUNDFORAGING SONGBIRD: THE WOOD THRUSH ................................................................... 42 5.3.4 MERCURY EXPOSURE BY FAMILY .............................................................................. 50 5.3.4.1 SONGBIRD CASE STUDY #6 - BICKNELL’S THRUSH ........................................ 52 5.3.5 BLOOD MERCURY CONCENTRATIONS AND REPRODUCTIVE SUCCESS ..... 54 5.3.5.1 SONGBIRD CASE STUDY # 7 - CAROLINA WREN .............................................. 55 5.4 CONCLUSIONS ................................................................................................................................ 57 6.0 BATS................................................................................................................................................................. 58 Biodiversity Research Institute

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6.1 STUDY AREA .................................................................................................................................... 58 6.2 METHODS ......................................................................................................................................... 58 6.3 RESULTS AND DISCUSSION ....................................................................................................... 58 6.3.1 SPECIES MERCURY EXPOSURE .................................................................................... 58 6.3.2 REGIONAL MERCURY EXPOSURE ............................................................................... 61 6.3.4 MERCURY EXPOSURE BY AGE AND SEX................................................................... 67 6.4 CONCLUSIONS ................................................................................................................................ 68 7.0 POLICY AND MANAGEMENT RECOMMENDATIONS .................................................................... 70 8.0 ACKNOWLEDGEMENTS ........................................................................................................................... 72 9.0 LITERATURE CITED .................................................................................................................................. 74 10.0 APPENDIX A – COMMON AND LATIN NAMES OF SONGBIRDS SAMPLED FOR BLOOD HG CONCENTRATIONS. .......................................................................................................................................... 89 11.0 APPENDIX B – SONGBIRD MERCURY EXPOSURE BY SPECIES .............................................. 92 12.0 APPENDIX C – SONGBIRD MERCURY EXPOSURE BY FAMILY ............................................... 96

LIST OF FIGURES Figure 1. Study area map of soil sampling locations. .......................................................................... 15 Figure 2. Mean plus standard deviation and maximum level detected of Hg in soil sampled in PA, VA, and four regions of NY. ................................................................................................................ 18 Figure 4. Relationship between pH and Hg concentrations in organic and mineral soil layers in samples (N = 31) collected at IES in Millbrook, NY ......................................................................... 19 Figure 5. Relationship between pH and exchangeable calcium (Ca) concentrations in organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY .......... 19 Figure 6. Relationship between pH and exchangeable potassium (K) in the organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY ................................... 20 Figure 7. Relationship between pH and exchangeable magnesium (Mg) in the organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY. .................................. 21 Figure 8. Invertebrate sampling locations in New England and the Mid-Atlantic States, 2005 to 2008, and 2010. ................................................................................................................................. 22 Figure 9. Mean plus standard deviation and maximum levels detected of MeHg concentrations in invertebrate orders sampled in New England and Mid-Atlantic States, 2005 to 2010. ....................................................................................................................................................... 24

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Figure 10. Regional means plus standard deviation and maximum levels detected of MeHg concentrations in Araneae species sampled in New England and Mid-Atlantic States, 2005 to 2010. ................................................................................................................................................................ 24 Figure 11. Map of Lake George, NY showing the location of Dome Island .................................. 26 Figure 12. Study area map of songbird sampling locations.............................................................. 30 Figure 13. Regional means plus standard deviations and maximum levels detected of blood Hg levels (ppm) in songbirds sampled in New England and Mid-Atlantic States, 1999 to 2007. ....................................................................................................................................................................... 31 Figure 14. Mean plus standard deviation and maximum level detected of blood Hg concentrations in songbirds sampled in Southwest VA, 2005 to 2007. ....................................... 33 Figure 15. Mean plus standard deviation and maximum level detected of blood Hg concentrations in songbirds sampled in Adirondack Mts, NY region, 2006 and 2007. .......... 33 Figure 16. Mean plus standard deviation and maximum level detected of blood Hg in Saltmarsh Sparrows sampled in coastal New England and Long Island, NY, 2000 to 2007. 35 Figure 17. Regional mean plus standard deviation and maximum level detected of blood Hg concentrations detected in Rusty Blackbirds in New England, 2007 to 2010. .......................... 37 Figure 18. Mean blood Hg level (ppm) by songbird foraging guild as defined by De Graaf et al. (1985). .............................................................................................................................................................. 40 Figure 19. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “omnivore ground” foraging guild species sampled in New England and Mid-Atlantic States, 2000 to 2007. .............................................................................................................. 41 Figure 20. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore ground” foraging guild species sampled in New England and the Mid-Atlantic States, 2004 to 2010. ...................................................................................................... 41 Figure 21. Relationship between the amount of exchangeable calcium in the organic and mineral soil layer and Wood Thrush (N = 6) blood Hg concentrations. ....................................... 43 Figure 22. The relationship between the amount of exchangeable Ca in the organic and mineral soil layers and blood Hg concentrations of Wood Thrushes (N = 6) ............................ 43 Figure 23. Mean plus standard deviation and maximum level detected of blood Hg concentrations among “insectivore air” foraging guild species sampled in New England and Mid-Atlantic States, 2005 to 2007. .............................................................................................................. 45

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Figure 24. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “omnivore ground/lower-canopy” foraging guild species sampled in New England and Mid-Atlantic States, 1999 to 2007. .................................................................................... 45 Figure 25. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore upper-canopy” foraging guild species sampled in New England and the Mid-Atlantic States, 1999 to 2010. ............................................................................ 46 Figure 26. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Louisiana Waterthrush and Northern Waterthrush sampled in New England and Mid-Atlantic States, 2005 to 2007. .................................................................................... 48 Figure 27. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore lower-canopy” foraging guild species sampled in New England and Mid-Atlantic States, 2004 to 2007. .................................................................................... 49 Figure 28. Mean plus standard deviation and maximum level detected of blood Hg concentrations among songbird families sampled in New England and Mid-Atlantic States, 1999 to 2010. ....................................................................................................................................................... 50 Figure 29. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Tyrannidae species sampled in New England and Mid-Atlantic States, 2005 to 2007. ....................................................................................................................................................... 51 Figure 30. Mean blood Hg concentration in Turdidae family species sampled in New England and Mid-Atlantic States, 1999 – 2008. ..................................................................................... 53 Figure 31. Regional means plus standard deviations and maximum levels detected of blood Hg concentrations Bicknell’s Thrush sampled in New England and New York, 1999 – 2007. ................................................................................................................................................................................... 54 Figure 32. Songbird species sampled in New England and the Mid-Atlantic States between 1999 and 2010 with individuals whose blood Hg (ppm, ww) concentrations put them at risk of reduced nesting success. ................................................................................................................... 56 Figure 33. Study area of bat sampling locations. ................................................................................... 60 Figure 34. Mean plus standard deviation and maximum level detected of fur Hg concentrations in bat species sampled in New England and Mid-Atlantic States, 2006 to 2008. ....................................................................................................................................................................... 61 Figure 35. Regional mean fur Hg concentrations in bats sampled in New England and MidAtlantic States, 2006 to 2008. ....................................................................................................................... 62 Figure 36. Mean and maximum level detected of fur Hg (ppm) in bats sampled near Little River, Rockingham County in Southeastern NH, 2008. ....................................................................... 63 Biodiversity Research Institute

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Figure 37. Regional mean fur Hg concentrations in Big Brown Bats sampled in New England and Mid-Atantic States, 2006 to 2008 ...................................................................................... 64 Figure 38. Regional mean fur Hg concentrations in Eastern Small-footed Myotis sampled in coastal ME, southern NY, and WV, 2006 to 2008. ............................................................................... 65 Figure 39. Regional mean and maximum levels detected of fur Hg concentrations in Indiana Bats sampled in New York State, 2006 to 2008..................................................................... 65 Figure 40. Regional means and maximum levels detected of fur Hg in Northern Long-eared Bats sampled in New England and Mid-Atlantic States, 2006 to 2008 ......................................... 65 Figure 41. Regional means and maximum levels detected of fur Hg concentrations in Eastern Pipistrelles sampled in WV and Coastal VA, 2007 and 2008. .......................................... 66 Figure 42. Regional means and maximum levels detected of fur Hg concentrations in Red Bat sampled in New England and Mid-Atlantic States, 2006 to 2008 ........................................... 66 Figure 43. Regional means and maximum levels detected of fur Hg concentrations in Little Brown Bats sampled in New England and Mid-Atlantic States, 2006 to 2008 .......................... 67 Figure 44. Mean fur Hg concentrations among male and female adult and juvenile bats sampled in New England and the Mid-Atlantic States, 2006 to 2008 ........................................... 68 Figure 45. Mean plus standard deviation of blood Hg concentrations in Cardinalidae species. ................................................................................................................................................................... 96 Figure 46. Mean and maximum level detected of blood Hg concentrations in Emberizidae species. ................................................................................................................................................................... 96 Figure 47. Mean and maximum blood Hg concentrations in Hirundinidae species. ............... 97 Figure 48. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Icteridae species. ........................................................................................................... 97 Figure 49. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Paridae species. .............................................................................................................. 98 Figure 50. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Parulidae species. .......................................................................................................... 98 Figure 51. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Sittidae species. .............................................................................................................. 99

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Figure 52. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Troglodytidae species. ................................................................................................. 99 Figure 53. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Vireonidae species. ..................................................................................................... 100

LIST OF TABLES Table 1. Carolina Wren blood, feather, and egg Hg effects concentrations associated with MCestimate-modeling reduction in nest success (adapted from Jackson et al. 2011). .......... 56

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1.0 EXECUTIVE SUMMARY Multiple environmental stressors such as acid rain, habitat degradation, and global climate change, are well established threats to biological diversity in North America. Recently, compelling investigations into the adverse impacts of mercury on wildlife indicate that mercury may be another pervasive and invisible risk to ecosystem health. Although great strides in the reduction of anthropogenically released mercury have been made, environmental loads continue to be of concern. Not only are new locations of high mercury concentrations (or biological mercury hotspots) being discovered, but taxa within foodwebs once thought safe are in danger. The following synthesis describes a hidden, or invisible, impact of methylmercury contamination across ecosystems in the northeastern United States— from Virginia to New York to Maine. We herein document and describe the potential adverse impacts of mercury to invertivores, such as songbirds and bats. While past investigations have rightly emphasized adverse impacts to fish-eating wildlife, such as Common Loons (Gavia immer), Bald Eagles (Haliaeetus leucocephalus), and River Otter (Lontra canadensis), recent findings by BRI researchers and their colleagues have now established that terrestrial food webs have great ability to biomagnify methylmercury to levels of conservation concern. This finding is not restricted to areas with waterborne point sources, such as industrial sites on rivers, but also reflects exposure in remote habitats through atmospheric deposition. Research has shown that mercury biomagnification within the invertebrate community, which comprises the prey base for the species highlighted in this report, is the critical link to understanding how mercury cycles through terrestrial ecosystems. As food chain length increases, we see higher levels of mercury in the top-level predators. We sampled approximately 80 songbird species from many different habitats that had blood mercury concentrations exceeding the current level of concern. Research has shown that the risk of methylmercury toxicity varies greatly depending on the physical, chemical, and biological components of an ecosystem. We found that species inhabiting wetland ecosystems, such as bog and beaver ponds (e.g., Rusty Blackbird (Euphagus carolinus)) or estuaries (e.g., Saltmarsh Sparrow (Ammodramus caudacutus)) are at the highest risk for mercury bioaccumulation. This does not, however, mean that birds in upland ecosystems are sheltered from mercury contamination; we also found mercury in the blood of species such as Bicknell’s Thrush (Catharus bicknelli), who live in high elevation forests thought to be removed from mercury contamination. Established effect levels remain undefined for bats, however evidence indicates that 10 ppm in the fur of bats correlates with biochemical changes in the brain. Seven out of nine Biodiversity Research Institute

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species of bat sampled in this study had individuals that exceeded this level of concern, indicating bats bioaccumulate mercury at high levels across many different ecosystems. Bats are considerably longer lived than most songbirds, making them more likely to build high levels of mercury over time. This investigation provides critical information to policy makers regarding the pervasiveness of environmental mercury pollution in the northeastern United States. The results from this study indicate that mercury levels in songbirds, bats, and invertebrates throughout the Northeast are high enough to cause detrimental effects to populations inhabiting areas prone to bioaccumulation of mercury in the terrestrial food web. Continued research should focus on the interaction of the multiple environmental stressors including mercury, climate change, and acid deposition. Modeling the impacts of these factors will help us better identify biological mercury hotspots and on-the-ground biomonitoring will allow us to validate the pathway of mercury in the environment through the food web.

2.0 INTRODUCTION Air pollution has been linked to adverse effects in wildlife (Lovett et al. 2009). Specifically, elevated levels of atmospheric sulfur (S), nitrogen (N), and mercury (Hg) deposition in the Northeastern United States have negatively influenced wildlife populations (Graveland 1990, Hames et al. 2002, Rimmer et al. 2005, Evers et al. 2008). Mercury, in particular, has been well-studied and observed to “biomagnify”, i.e., increase in concentration, and thus toxicity, with increasing trophic level within a food web; however, most of the investigations have been focused on freshwater aquatic ecosystems (Evers et al. 2005, Chen et al. 2005, Kamman et al. 2005, Pennuto et al. 2005). Despite the recent documentation of elevated Hg exposure in terrestrial biota, relatively little is known about pathways for Hg uptake and transfer in upland ecosystems (Cristol et al. 2008, Rimmer et al. 2010). Globally, the inventory of mercury in surface soils far exceeds that in the aquatic and atmospheric compartments (Wiener et al. 2003). The vast majority (947Mmol) of the estimated total mass of mercury released to the environment in the past century resides in surface soils, compared to 17 Mmol in the atmosphere and 36 Mmol in the oceans (Wiener et al. 2003). Consequently, in order to understand mercury cycling in the terrestrial environment, one must consider the role of soil and what factors influence Hg retention and release to surrounding watersheds and uptake by biota at the base of the food web. And then, to truly disentangle mercury’s effects on ecosystem structure and function, it is important to consider how factors that influence Hg chemistry in the soil profile act in other ways to affect soil structure and function. Biodiversity Research Institute

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The different chemical forms of Hg in the atmosphere have varying residence times (hours to months) and transport distances (local to global) (Driscoll et al. 2007, Lovett et al. 2009). Highly soluble Hg (II) species are quickly stripped from the atmosphere and deposited locally, whereas aerosol (Hg-p) emissions are transported regionally, and elemental (Hg0) emissions are transported globally (Keeler et al. 1995, Lindberg and Stratton 1998, Schroeder and Munthe 1998, Demers et al. 2007). Litterfall and throughfall deliver different forms of mercury to the forest floor. Gaseous elemental mercury (Hg0) contacting leaf surfaces is either re-emitted to the atmosphere or taken up by stomata and retained internally by the leaf tissue until deposited in litterfall (Mosbaek et al. 1988, Demers et al. 2007). Reactive Gaseous Mercury (Hg(II)) and Hg-p are adsorbed to the leaf surface during dry deposition and may be leached from those surfaces during precipitation events, contributing to elevated mercury levels in throughfall (Iverfeldt 1991, Kolka et al. 1999, Rea et al. 2000, 2001, Demers et al. 2007). Additionally, Rimmer et al. (2005) cited numerous studies that have demonstrated that methylmercury (MeHg),the toxic form of mercury, is present in both live and recently senesced forest foliage in proportions of approximately 1% of the total Hg content (e.g., Lee et al. 2000, Schwesig and Matzner 2000, St. Louis et al. 2001, Ericksen et al. 2003). The speciation of mercury in most upland soils is probably dominated by divalent mercury species that are sorbed primarily to organic matter in the humus layer and secondarily to mineral constituents in the soil (Lindquvist 1991, Kim et al. 1997, Wiener et al. 2003). The availability of Hg (II) to organisms is determined by its activity in soil solution, which is, in turn, controlled by both the solid and solution phase characteristics of the soil (Jing et al. 2007). Many environmental factors can interfere with the Hg adsorption-desorption process, which include: Hg speciation, soil pH, chloride ions, organic matter content, form and content of soil colloids, and competitive inorganic ions, etc. (Jing et al. 2007). Therefore, fine, spatial-scale patterns such as local variation in vegetation type (receptor surface) and microclimate may be important determinants of the watershed-scale capture of atmospheric mercury (Miller et al. 2005) . Acid rain, i.e., wet atmospheric deposition of acidifying industrial emissions, such as nitrogen and sulfur oxides, is one such mechanism that reduces soil pH and can thereby increase metal mobility and availability in soils. Jing et al. (2007) found a direct correlation between decreasing soil pH and increasing retention of heavy metals, such as Hg. In addition to increasing Hg and other heavy metal mobility, acid deposition can also contribute to the methylation of mercury. Soil chemistry promotes methylation when soils are low in oxygen (usually saturated soils), high in sulfur, and high in dissolved organic carbon. Sulfate-reducing bacteria that convert elemental Hg to MeHg thrive in these Biodiversity Research Institute

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conditions, and thus, pollution causing acid deposition, especially of nitrogen and sulfur oxides, enhances soil conditions for the methylation process (Scheuhammer 1987). Methylmercury in the leaf-litter and forest floor is available to invertebrates, such as gastropods, isopods, and insects. The incorporation of MeHg from the leaf litter by detritivores and by predaceous invertebrate species (i.e., centipedes and spiders) that feed on detritivores is a direct pathway to elevated Hg exposure for the next highest trophic level, invertivores (i.e., songbirds and bats). Spiders can have a particularly influential impact on biomagnifying MeHg in forest food webs. In Virginia, Cristol et al. (2008) found that some terrestrial-feeding songbird species that preyed on spiders had Hg levels that exceeded those of aquatic-feeding songbirds. Even piscivorous species, such as the Belted Kingfisher (Megaceryle alcyon), had lower Hg body burdens than terrestrial songbird species in that study. Terrestrially acidified environments not only enhance methylmercury availability, they reduce calcium availability. Correlations between increased Hg input and decreased soil pH and calcium availability can have important ramifications on songbird breeding success, particularly egg production and growth of hatchlings. Indeed, acid rain has been linked by a number of studies to declines of bird species in Europe and the United States (Graveland 1990, Möckel 1992, Graveland 1998, Zang 1998, Hames et al. 2002). This phenomenon may be linked to depletion of soil pools of extractable calcium by leaching (Likens et al. 1996, Driscoll et al. 2001), leading to decreases in the abundance of calcium-rich invertebrate prey essential to breeding female birds as sources of calcium during egg production and when feeding nestlings (Graveland 1996, Graveland and Drent 1997, Bures and Weidinger 2003). Logistic regression analysis of habitat-related variables measured by Hames et al. (2002) indicated a strong, negative relationship between acid rain and the probability of detecting Wood Thrush (Hylocichla mustelina) breeding evidence. Additionally, uptake and toxicity of trace metals from food have both been shown to increase in the presence of low dietary calcium and may play an important, but as yet undocumented, role in regional declines of terrestrial bird species (Scheuhammer 1991, Silver and Nudds 1995, Scheuhammer 1996). There have been very few investigations on Hg exposure in bats; however, they appear to be capable of accumulating very high levels of Hg in their blood and fur. Miura et al. (1978) examined various species of Chiroptera from areas in Japan sprayed with Hg fungicides and found total fur Hg levels of approximately 33 ppm (fw). Bats may be exposed to mercury in both industrialized and rural areas. Pipistrelle Bats (Pipistrellus pipistrellus) had elevated levels of metals, including Hg, and pesticides in both industrial and rural areas in Sweden (Gerell and Lundberg 1993). In Great Britain, Pipistrelle Bats showed a significant positive Biodiversity Research Institute

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trend in Hg levels over a 15-year period indicating a potential relationship with increased atmospheric inputs and/or exposure to point sources (Walker et al. 2007). Bats are increasingly of high conservation concern to conservation agencies and other entities. Mercury is one anthropogenic stressor on bat populations that may be compounded by other stressors such as wind turbines and white-nose syndrome, a disease that has caused mass mortality among hibernating bats throughout New England and the Mid-Atlantic States over the last four years. Therefore, high resolution investigations to determine spatially explicit effects from Hg on reproductive success, survival, and physiological effects are of great importance and urgency. There are several factors that increase bats’ risk of exposure to and accumulation of mercury: (1) they are long-lived, (2) they feed at relatively high levels in the trophic food web, and (3) they are very mobile in comparison to other mammals of similar size. In the interest of assessing potential impacts and injury to invertivores from atmospheric Hg deposition, we established a network of sampling stations in New England and the MidAtlantic States to assess Hg concentrations in soil, invertebrates, songbirds, and bats in terrestrial habitats. We addressed not only the importance of spatial-scale variation of Hg levels within ecosystems but also finer scale gradations between species, family groupings, and foraging guilds. Our overall objective for performing this research was to identify invertivore species prone to elevated Hg levels. Landscape characteristics shape the ultimate fate of Hg deposited within an ecosystem and these geochemical processes have not been well quantified. However, by determining background Hg levels in terrestrial species across a wide geographic area in locations that are not directly affected by point source mercury emissions, then we can begin to identify geographic areas, habitats, taxonomic groups, and natural communities at greatest ecotoxicological risk from mercury deposition. This information can be used to inform policy makers concerned with local, regional, and national air quality issues.

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3.0 SOILS 3.1 STUDY AREA Soil was opportunistically collected at mistnet lanes where songbirds and invertebrates were sampled in NY, PA, and VA (Figure 1).

Figure 1. Study area map of soil sampling locations. 3.2 METHODS Soil samples were analyzed for total Hg at Syracuse University, Syracuse, NY using a direct mercury analyzer. Samples collected at the Institute for Ecosystem Studies (IES) in Millbrook, NY were analyzed for total Hg as well as exchangeable calcium (Ca), available Ca, pH, moisture (%), potassium (K), and magnesium (Mg). Statistical analysis was performed using Program JMP 9.0. Nonparametric Spearman’s rank correlation was used to Biodiversity Research Institute

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determine relationships between soil variables, including soil moisture, pH, Hg, Ca, K, and Mg. Relationships were considered significant at P < 0.05. 3.3 RESULTS AND DISCUSSION 3.3.1 MERCURY LEVELS IN SOIL Mercury levels in soil samples (N = 62) ranged from 0.06 ppm to 0.69 ppm (Figure 2). Soil collected in the Adirondack Mts, NY, had the highest mean soil Hg concentration ( = 0.25 ppm). The highest soil Hg level detected (0.70 ppm) was collected near Arbutus Lake, Adirondack Mts, NY. Within that region, elevated soil Hg levels were also detected in the Tug Hill Plateau (0.39 ppm), Elk Lake (0.24 ppm), Ferd’s Bog (0.19 ppm), and Spring Pond Bog (0.10 ppm); the lowest level was detected at Sunday Lake (0.09 ppm). Plateau Mt. in the Catskills Mts, NY had the highest soil Hg level (0.35 ppm) collected in that region followed by Devil’s Tombstone Campground (0.27 ppm), Lake Capra (0.22 ppm), and Hunter Mt. (0.12); the lowest levels were collected at Emmons Bog (0.08 ppm), Neversink Valley (0.07 ppm), and Belle Ayr Fish Hatchery (0.07 ppm). The highest level from samples collected in the Southern NY region was from the Sam’s Point Preserve in the Shawangunk Mts. (0.28 ppm) followed by Black Rock Forest (0.27 ppm); the lowest level observed was at Mohonk Preserve (0.09 ppm). VA samples were collected at the Buller Fish Hatchery (0.06 ppm) and Clinch Mt. (0.23 ppm). PA soil samples were collected at Powdermill; a forest sample was 0.10 ppm and a sample from Spruce Bog was 0.23 ppm. Central/Western NY soil samples were collected at Allegany State Park (0.10 ppm) and Brookfield Railroad State Forest (0.09 ppm). The wide ranges in soil Hg at sites within the same geographic region and/or landscape, e.g., Sam’s Point and Mohonk Preserve in the Shawankgunk Mts., Southern NY, are likely related to landscape characteristics. Indeed, variables such as soil moisture and chemistry play important roles regarding the ultimate fate of Hg in soil.

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Soil Hg (ppm)

1.0 0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2 0.0

Soil Sampling Regions

Figure 2. Mean plus standard deviation and maximum level detected of Hg in soil sampled in PA, VA, and four regions of NY. Small sample sizes precluded statistical comparisons. 3.3.2 CASE STUDY # 1 - FOREST SOILS 3.3.2.1 SOIL MOISTURE Soil moisture plays an important role in methylation of mercury. Increased soil moisture creates a suitable environment for sulfate- and iron- reducing bacteria that transform mercury to its bioavailable form, methylmercury (MeHg) (Wiener et al. 2003). Mercury accumulation in soils has most often been studied in aquatic ecosystems where production of MeHg is favored due to the anaerobic conditions of saturated soil. Preliminary research suggests that MeHg is not as readily formed in terrestrial soils as compared to wetland soils; however, as our research illustrates, MeHg is prevalent throughout the terrestrial food web. Soil samples were collected at the Institute for Ecosystem Studies (IES) in Millbrook, NY were analyzed for moisture content and Hg concentrations. Nonparametric Spearman rank correlation analysis detected a significant positive relationship between organic soil layer moisture and Hg concentrations; no significant trend was detected in the mineral soil layer Biodiversity Research Institute

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(Figure 3). Soil moisture also helps facilitate diffusion of nutrients, such as Ca, K, and Mg, across soil gradients. Diffusion is the primary mechanism by which these vital nutrients are delivered to root systems for uptake by plants. There was a significant and positive relationship between calcium and soil moisture in the organic soil layer, and no significant relationship in the mineral soil layer (organic: Spearman’s ρ = 0.45, P = 0.02; mineral: Spearman’s ρ = 0.15, P = 0.56). We did not detect any significant relationships in our samples between soil moisture and K (organic: Spearman’s ρ = 0.20, P = 0.34; mineral: Spearman’s ρ = 0.21, P = 0.42) or Mg (organic: Spearman’s ρ = 0.17, P = 0.42; mineral: Spearman’s ρ = 0.31, P = 0.23). 300

Organic Mineral

Soil Hg (µg/kg)

250 200 150 100 50 0 0

20

40

60

80

Soil Moisture (%)

Figure 3. The relationship between moisture and Hg concentration in the organic and mineral soil layers from samples (N = 31) collected at IES in Millbrook, NY (organic soil layer: Spearman’s ρ = 0.59, P = 0.02; mineral soil layer: Spearman’s ρ = - 0.23, P = 0.38). 3.3.2.2 SOIL CHEMISTRY Soil pH is an indication of the acidity or alkalinity of soil. It is measured in pH units ranging from the most acidic, 0.0, to the most alkaline, 14.0, with 7.0 being neutral. Most plants grow best in a soil pH of 6.0 to 7.0, although, some plants can tolerate levels above or below this range. Normal soil pH ranges between 5.0 and 8.0 and levels below that range are considered highly acidic. Acid rain causes soil to become acidic due to deposition of hydrogen ions and by mobilization of aluminum ions, both of which displace basic cations, such as Ca, Mg, and K, which are then leached out of the organic and mineral soil layers. Ca, Mg, and K are mineral nutrients that are vital to plant growth and health and may be less available in soils with low pH. Additionally, acidic soils tend to be associated with higher retention of heavy metals, such as Hg (Jing et al. 2007). Our findings indicated that acidic soils had higher levels of mercury and there was a significant correlation between acidity Biodiversity Research Institute

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and mercury concentration in the organic soil layer; no significant relationship was detected between soil pH and Hg in the mineral soil layer (Figure 4). Calcium levels in the mineral soil layer exhibited a strong significant tendency to increase with decreasing acidity, but there was no correlation between pH and calcium in the organic soil layer (Figure 5). 300

Organic Mineral

Soil Hg (µg/kg)

250 200 150 100 50 0 0

1

2

3

4

5

6

7

Soil pH

Figure 4. Relationship between pH and Hg concentrations in organic and mineral soil layers in samples (N = 31) collected at IES in Millbrook, NY (organic soil layer: Spearman’s ρ = 0.81, P = 0.0002; mineral soil layer: Spearman’s ρ = - 0.15, P = 0.57).

Soil Exchangeable Ca (cmolc/kg)

12 Organic

Mineral

1

2

10 8 6 4 2 0 0

3

4

5

6

7

Soil pH

Figure 5. Relationship between pH and exchangeable calcium (Ca) concentrations in organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY (organic soil layer: Spearman’s ρ = 0.27, P = 0.18; mineral soil layer: Spearman’s ρ = 0.80, P = 0.0001). Biodiversity Research Institute

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Our results also indicated an inverse relationship between available K and Mg and acidity in the mineral soil layer; no significant relationships were detected in organic soil layer samples (Figures 6 & 7). Potassium is a primary macronutrient and is consumed in large quantities by plants to help in protein building, photosynthesis, fruit production, and disease prevention. Magnesium is a micronutrient and is consumed in smaller quantities but it is part of the chlorophyll necessary for photosysnthesis and also plays a role in activating enzymes necessary for plant growth. These elements were strongly correlated with one another in our soil samples (Spearman’s ρ = 0.75, P < 0.0001). They were also each strongly correlated with the amount of available Ca (Mg to Ca: Spearman’s ρ = 0.84, P < 0.0001; K to Ca: 0.54, P = 0.0002). In addition to calcium’s role in uptake by invertebrates that provide calcium needs required by breeding birds, it is a vital nutrient for plant health. Calcium is a critical component of plant cell wall structure, which faciliates transport and retention of other elements, and provides strength in the plant. However, these valuable nutrients are less available in acidic soils due to leaching out (Nihlgard 1985). Therefore, to uncover mercury’s effect on ecosystem structure and function, it is important to consider other interacting ecological stressors which may be at play. Such is the case where acidifying emissions have the ability to drastically alter the chemical structure of soils and plants, and thereby affect Hg mobility and availability in soil.

Soil Exchangeable K (cmolc/kg)

2.5

Organic Mineral

2.0 1.5 1.0 0.5 0.0 0

1

2

3

4

5

6

7

Soil pH

Figure 6. Relationship between pH and exchangeable potassium (K) in the organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY (organic soil layer: Spearman’s ρ = -0.31, P = 0.13; mineral soil layer: Spearman’s ρ = 0.47, P = 0.05).

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Soil Exchangeable Mg (cmolc/kg)

4.5 Organic

4.0

Mineral

3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 0

1

2

3

4

5

6

7

Soil pH

Figure 7. Relationship between pH and exchangeable magnesium (Mg) in the organic and mineral soil layers in samples (N = 42) collected at IES in Millbrook, NY (organic soil layer: Spearman’s ρ = -0.33, P = 0.10; mineral soil layer: Spearman’s ρ = 0.61, P = 0.009).

3.4 CONCLUSION Deposition of acidifying emissions and heavy metals has a profound effect on forest ecosystems. Acid rain is a complex solution of primarily H+, SO42- , NH4+, and NO3- pollutant ions. Vegetation damage may occur through direct exposure to air pollutants or acidification of soil. Acid-induced leaching of plant nutrients, primarily magnesium and potassium, may result in reduced forest health. Additionally, leaching may be responsible for a 50% loss of calcium pools in soils over the last 50 years (Likens et al. 1996). Once the soil is acidified, it is prone to acidifying nearby surface waters and retaining elevated levels of toxic heavy metals, such as aluminum and mercury. The pathways for accumulation of mercury in terrestrial ecosystems are not fully understood, but recent work suggests that accumulation involves absorption of gaseous mercury (Hgº) by foliar tissue of deciduous trees (Ericksen et al. 2003, Frescholtz et al. 2003) and needles in coniferous trees, with subsequent release of mercury in litterfall (Rea et al. 2002, Ericksen et al. 2003, Frescholtz et al. 2003). While litterfall may represent the bulk of mercury input to forested ecosystems, the wash-off of dry-deposited Hg species in throughfall, direct deposition in precipitation, and uptake of dissolved mercury by roots and translocation to foliar tissue may also play roles (Rea et al. 2002). Litterfall and throughfall deliver different forms of mercury to the forest floor and this may strongly influence the retention of mercury and its ultimate fate in terrestrial ecosystems. In any case, total mercury (THg) inputs to eastern forests are largely incorporated in the leaf-litter and topmost layers of soils, where it is available to invertebrate detritivores, such as gastropods (snails and slugs), isopods (woodlice), myriapods (millipedes), and to soil-dwelling annelids (earthworms). Biodiversity Research Institute

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Therefore, we must also monitor Hg concentrations in invertebrate species to positively identify the soil and leaf litter layers as significant pathways for Hg to enter the food web.

4.0 INVERTEBRATES 4.1 STUDY AREA Invertebrates were opportunistically collected along mist net lanes at songbird sampling stations in ME, NH, NY, PA and WV (Figure 8).

Figure 8. Invertebrate sampling locations in New England and the Mid-Atlantic States, 2005 to 2008, and 2010. 4.2 METHODS Four wet cardboard traps, each placed 20 m from the center point of the site in the four cardinal directions were used to sample invertebrates in the leaf litter. Each trap was a 1 ft. x 1 ft. (30.5 cm x 30.5 cm) square of plain (uncoated) corrugated cardboard. At least one side, which was placed downward, was free of printing or glue. The traps were placed in the afternoon or evening and checked the following morning. Each trap was set by holding the cardboard at an angle of about 45° with one side touching the ground and then slowly Biodiversity Research Institute

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pouring approximately 1 liter of non-chlorinated water across the top surface of the cardboard. The cardboard was then placed (wet side down) in the wet area in the leaf litter where the excess water ran off. A few sticks or stones were placed on top of each trap to hold it in place. Additional invertebrates were collected by using pitfall traps that were left out for varying lengths of time. Specimens were collected and stored in 95% ethyl alcohol until they were analyzed for MeHg content, which was reported as parts per million dry weight (ppm, dw) content. 4.2.1 STATISTICAL ANALYSIS Statistical analysis was conducted in JMP 9.0. Arithmetic means are presented in graphs; however, invertebrate Hg concentrations were log-transformed prior to statistical analysis and checked for normality with the Shapiro-Wilk test. Homogeneity of variance was examined in normal data sets with the Bartlett’s test and in non-normal data sets with the Fligner-Killeen test, which is less sensitive to outliers. If normality and equal variance assumptions were met, differences between groups (e.g., sampling regions) were checked with t-tests or ANOVA and Tukey’s honestly significant difference test. Non-normal datasets with equal variance among groups were examined with the nonparametric Kruskal-Wallis and Wilcoxon rank sum tests. Tests were considered significant at P < 0.05. 4.3 RESULTS AND DISCUSSION 4.3.1 SAMPLING EFFORT During 2005 to 2010, we sampled 371 invertebrates from 13 orders in 9 regions of New England and the Mid-Atlantic States. Diptera, Amphipoda, and Araneae species had the highest mean MeHg concentrations (Figure 9). 4.3.2. REGIONAL AND SPECIES MERCURY EXPOSURE All Dipteran and Amphipoda samples were collected in salt marsh habitat in coastal MA (Parker River NWR) and coastal ME (Rachel Carson NWR). Those collected in coastal MA had significantly higher MeHg concentrations compared to those collected in coastal ME [Diptera: MA ( = 0.39 ± 0.22 ppm, N = 29) vs. ME ( = 0.17 ± 0.08 ppm, N = 25), (P < 0.0001); Amphipoda: MA ( = 0.29 ± 0.11 ppm, N = 15) vs. ME ( = 0.26 ± 0.49, N = 15), (P < 0.0001)]. Additionally, Araneae spiders species collected in coastal MA had significantly higher MeHg levels than all other regions where they were sampled (P < 0.0001) (Figure 10).

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2.5

MeHg (ppm), dw

2.0

Maximum Level Detected Mean + SD

1.5 1.0 0.5 0.0

Figure 9. Mean plus standard deviation and maximum levels detected of MeHg concentrations in invertebrate orders sampled in New England and Mid-Atlantic States, 2005 to 2010. 1.4

MeHg (ppm), dw

1.2

Maximum Level Detected Mean + SD

1.0 0.8 0.6 0.4 0.2 0.0 Catskill Mts, NY (N = 15)

PA (N = 10)

Coastal ME (N = 13)

Southern NY (N = 18)

Coastal MA (N = 14)

Adirondack Mts, NY (N = 115)

Araneae Sampling Regions

Figure 10. Regional means plus standard deviation and maximum levels detected of MeHg concentrations in Araneae species sampled in New England and Mid-Atlantic States, 2005 to 2010. Coastal MA Araneae species had significantly higher MeHg concentrations compared to other sampling locations (P < 0.0001). Biodiversity Research Institute

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Invertebrates sampled from Parker River NWR likely exhibited such high Hg levels because sampling efforts were concentrated in the salt marsh situated between the Merrimack and Parker Rivers. Both rivers carry waters from interior watersheds to the coast. The middle and lower Merrimack River is a well known Hg hotspot due to high atmospheric deposition rates and historic point source pollution (Evers et al. 2007). Benthic fauna, such as amphipods, are good indicators of soil contamination. Amphipods are bottom-dwellers that filter-feed on suspended particulate matter and deposit feed on detritus and sediment. Therefore, they are at high risk to toxin accumulation due to their proximity and long-term exposure to soil pollution (DeWitt et al. 1992). George et al. (2001) found that amphipods contained higher concentrations of Hg than other higher trophic level organisms, such as odonates and crayfish. The bioavailability of MeHg in benthic organisms at contaminated sites appears to reach a seasonal high during summer and autumn months (Zizek et al. 2007). This seasonal variability increases the potential for magnification of mercury in higher trophic levels, particularly in songbirds, many of which have breeding season diets reliant on invertebrate prey. The proportion of bioavailable MeHg to THg in predatory invertebrates that prey upon other predatory invertebrates, e.g., heteropterans, coleopterans, odonates, is 70% to 95%, compared to 35% to 50% in detritivores-grazers (dipterans, ephemeropteran, trichopterans) (Tremblay et al. 1996). Therefore, predatory invertebrates are at great risk of Hg accumulation. Indeed, Tremblay et al. (1996) found that MeHg concentrations in predatory invertebrates were 3 times greater than levels found in detritivores. They attributed several abiotic factors, including temperature, oxygen concentration, atmospheric deposition and the organic content of the sediment, as determining factors of the availability of MeHg to low trophic level organisms. Dipteran samples in this study were primarily from the Tabanus genus, which are blood-sucking horse flies that fall into the predatory invertebrate category. Rimmer et al. (2010) studied Hg levels of invertebrates in a montane forest habitat and found a mean THg level in Dipterans of 0.11 ± 0.17 ppm and range of 0.002 to 0.982 ppm. Spiders are also predatory invertebrates and those sampled at coastal sites and in the Adirondack Mts, NY, had the highest mean MeHg concentrations among sampling regions. MeHg concentrations in spiders ranged from 0.006 ppm, dw (Dome Island, NY) to 2.02 ppm (Rachel Carson NWR, ME). The highest MeHg levels in spiders in the Adirondack Mts were primarily from species collected on Dome Island in Lake George, which is discussed in greater detail below in Case Study # 2.

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4.3.3 CASE STUDY # 2 -DOME ISLAND SPIDERS (BUCK ET AL. 2011) Lake George is a large (114 km2) mesooligotrophic lake in northeastern New York and is in the southeastern most portion of Adirondack Park. Dome Island, located within the southern basin, is a small island (~6.1 hectares) with approximately 1100 m of shoreline. It is the highest elevated island on Lake George and nearly one mile from the nearest mainland (Figure 11). The island is a mix of deciduous and coniferous forest, such as red maple (Acer rubrum), paper birch (Betula papyrifera), white pine (Pinus strobus) and eastern hemlock (Tsuga canadensis).

Figure 11. Map of Lake George, NY showing the location of Dome Island in the southern basin (inset map shows the location of Lake George in northwest NY state). All observed spiders along transect lines were collected yielding a sample size of 309 spiders, representing 8 different families and 4 different foraging guilds. Individual spiders from the same transect and taxonomic families were composited to provide sufficient mass for a combined analysis of total mercury, methylmercury, and stable carbon and nitrogen isotopes. This resulted in a total of 81 spider samples. Total and methylmercury were analyzed to provide information about differences in Hg exposure across sites and across foraging guilds. Stable isotopes were analyzed to provide information about food web structure and the transfer of contaminants between trophic levels. Biodiversity Research Institute

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Total mercury (THg) concentrations measured in spiders ranged from 0.040 ppm, dry weight (dw), to 1.63 ppm, dw, with an overall mean concentration of 0.254 ppm, dw. The amount of highly bioavailable methylmercury (MeHg) in spiders ranged from 33.5 ± 8.1% to 52.7 ± 6.4% of THg. These values are higher than reported THg concentrations for spiders from forested areas in southern Vermont not affected by point source pollution (Rimmer et al. 2010; mean THg = 0.173 ppm, dw), but are lower that mean THg concentrations in spiders from the South River, Virginia, a river impacted by point source mercury pollution for many decades (Cristol et al. 2008; mean THg = 1.24 ppm, dw). The most abundant foraging guild of spider collected from Lake George sites were Orbweaving spiders (Families Tetragnathidae and Araeidae). These spiders are abundant in riparian and littoral zone habitats and, along with Cursorial predatory spiders (e.g., Family Lycosidae), have been the focus of other contaminant studies linking terrestrial and aquatic ecosystems (Cristol et al. 2008; Walters et al. 2010). Orb-weaving spiders collected at water’s edge sites on islands (combined data from Crown and Dome Islands) had significantly higher THg concentrations than the Mainland water’s edge site. Changes in the nitrogen isotopic concentration (δ15N) of spiders reflect changes in food web complexity and trophic level interactions and when examined in concert with mercury, provide an integrated assessment of contaminant transfer and biomagnification up through a food web. There is a strong correlation (r = 0.565) between the %MeHg and δ15N of Orb-weaving spiders collected from the water’s edge transects. Orb-weaving spiders from the water’s edge are the only sub-group of spiders where this relationship had a strong correlation. Overall these results suggest that bioaccumulation of Hg in Orbweaving spiders along the water’s edge is related to increasing food web complexity and suggests there may be a Hg pathway linking the adjacent aquatic environment to terrestrial food webs. High levels of mercury in the songbirds and spiders from BRI’s previous work at Dome Island raised concerns that high levels of mercury deposition were occurring at the site. To address this question, we acquired one of the few portable wet Hg deposition collectors in the country, and stationed it at Lake George during September-October 2009. Weekly wet Hg deposition data for Lake George ranged between 7.5 and 205.6 ng/m2. These data exhibit similar weekly trends as data from other long-term Hg deposition monitoring sites in NY State, suggesting that Hg deposition is not a primary driver for the high Hg concentrations observed in biota of Dome Island. A consistent challenge with Hg exposure studies is not only quantifying how much Hg is being deposited, but identifying potential sources of the Hg that is entering the ecosystem. Biodiversity Research Institute

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While advances are being made to differentiate Hg sources using stable Hg isotopes within food webs that have only two end members (e.g., Senn et al. 2010), to date, this has not been done successfully with atmospheric sources, largely due to the multiple sources of Hg that contribute to the atmospheric Hg pool and the difficulty with separating out sources within a multi-end member model. However, an exhaustive literature review of potential Hg sources within the Adirondacks region suggests that Hg sources can be divided into four primary contributors including: (1) natural emissions, (2) New York-based industrial sources, (3) U.S.-based sources; and (4) Hg emitted from sources within the Asian continent (Seigneur et al. 2003). The timing and associated weather pattern of precipitation events can also influence the degree to which local versus regional/global sources influence Hg deposition in the Adirondacks region (Choi et al. 2008). For some lakes in the Adirondacks region, local and regional emissions sources can account for as much as 80% of the total Hg flux (Bookman et al. 2008). We present a summary of potential local emissions sources proximate to Lake George including local aggregate and cement producing plants. Reductions of Hg emissions from local sources can result in significant reductions of Hg in biota (Evers et al. 2007; Hutcheson et al. 2008) and a continued effort that combines a science-based program with local community engagement and clear communication with local- and national-level policy makers can result in greater reductions in Hg emissions and the reduction of human and ecological health risks associated with Hg pollution. 4.4 CONCLUSION The detritus food web is the likely source of elevated Hg levels in soil-dwelling invertebrates. In the case of the salt marsh ecosystem, we saw that soil-dwelling isopods were capable of accumulating exceptionally high Meg levels from the detritus food web. Higher Hg concentrations detected in predatory invertebrates, such as spiders and bloodsucking flies, represent possible mechanisms of bioaccumulation within lower trophic levels of the food web. The biological significance of these findings are the implications these elevated MeHg levels have on higher trophic levels that feed on invertebrates, including fish, bats, and songbirds. While the role of elevated Hg in fish and the negative effects it has on both human and wildlife health have been and continue to be well-studied and documented, the repercussions of elevated Hg in bats and songbirds, particularly those in terrestrial habitats, are less recognized and poorly understood. Soil- and litter-dwelling invertebrates may comprise a significant portion of the diet of litter-feeding birds, with snails and slugs estimated to comprise 2.5% of the animal biomass and 6% of the available energy (Hawkins et al. 1997) in boreal forest ecosystems. Some of these invertebrates (snails, woodlice, millipedes and centipedes) may also represent crucial sources of calcium to many breeding birds (Graveland and van der Wal 1996, Bures and Weidinger 2003) and the abundance of all of these potential prey species Biodiversity Research Institute

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decline with declines in soil pH (Graveland 1996, Graveland and van der Wal 1996, Bures and Weidinger 2003). Indeed, healthy soil and invertebrates are critical building blocks necessary for survival of all vertebrate animals. In the next section, we will expand our sampling locations and explore Hg pathways in songbird species, habitats, and foraging guilds.

5.0 SONGBIRDS 5.1 STUDY AREA Songbirds were sampled at 165 locations in 11 New England and Mid-Atlantic States: Connecticut, Delaware, Maine, Massachusetts, New Hampshire, New York, Pennsylvania, Rhode Island, Vermont, Virginia, and West Virginia (Figure 12). 5.2 METHODS Sampling efforts were timed for June and July to allow time for depuration of Hg body burdens that could reflect winter and/or migratory MeHg uptake. It is well established that blood reflects recent dietary uptake of MeHg (Evers et al. 2005). Typically, 8 to 10, 12 m mist nets with a 36 mm mesh size were used to catch songbirds. Nets were placed on bamboo and/or metal poles. The nets were checked every 20 to 40 minutes. Captured birds were removed and placed in cotton holding bags until processed. All birds were released unharmed 15 to 45 minutes after capture. Birds were captured during both dawn and dusk periods. All birds were measured using standard wing, tail, tarsi, bill, and mass measurements, and banded with USGS bands. For all birds, 28-gauge disposable needles were used to puncture a cutaneous ulnar vein in the wing to collect a small blood sample. Each blood sample was collected in a 75 uL capillary tube, which was then sealed on both ends with Crito-seal or Critocaps ® and placed in a labeled plastic 7 cc vacutainer. Generally, 2 to 4 capillary tubes half-filled with blood were taken from each bird. The feathers were placed in a labeled plastic bag. All samples were stored in a field cooler with ice, and samples were later transferred for temporary storage (blood in the freezer, feathers in the refrigerator). Samples were analyzed for total mercury (THg) and reported as parts per million wet weight (ppm, ww). THg approximates MeHg, which is 90 to 100% of THg in avian blood (Rimmer et al. 2005). 5.2.1 STATISTICAL ANALYSIS Statistical analysis was conducted in JMP 9.0. Arithmetic means are presented in graphs; however, blood Hg concentrations were log-transformed prior to statistical analysis and checked for normality with the Shapiro-Wilk test. Homogeneity of variance was checked with Bartlett’s test. If normality and equal variance assumptions were met, differences between groups were checked with t-tests or ANOVA and Tukey’s honestly significant difference test. Non-normal datasets with equal variance among groups were examined with the nonparametric Kruskal-Wallis and Wilcoxon rank sum tests (p < 0.05). Biodiversity Research Institute

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Figure 12. Study area map of songbird sampling locations.

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5.3 RESULTS AND DISCUSSION 5.3.1 SAMPLING EFFORT

Mean Blood Hg (ppm), ww

A total of 1,878 songbirds representing 78 species were sampled at 165 locations within 20 geographic regions of New England and Mid-Atlantic States (Figure 13). Sample sizes of each species ranged from 1 to 494 and blood Hg levels ranged from 0.0005 ppm (American Goldfinch, Spinus tristis) to 3.73 ppm (Saltmarsh Sparrow, Ammodramus caudacutus). 4.0 3.5 3.0

Maximum Level Detected Mean + SD

2.5 2.0 1.5 1.0 0.5 0.0

Songbirds Sampling Areas

Figure 13. Regional means plus standard deviations and maximum levels detected of blood Hg levels (ppm) in songbirds sampled in New England and Mid-Atlantic States, 1999 to 2007. 5.3.2 REGIONAL AND SPECIES MERCURY EXPOSURE Mercury hotspots are geographic locations with disproportionately elevated Hg levels (Evers et al. 2007). The mechanisms that drive these trends include elevated atmospheric Hg deposition, high landscape sensitivity, large water-level manipulations, and direct Hg input from water discharges and contaminated soils. Abiotic and biotic features of sites with these characteristics are predicted to have elevated Hg levels corresponding with the rate of deposition and degree of landscape sensitivity and disturbance. We focused our sampling at sites not associated with direct point source Hg pollution in order to determine background Hg levels in songbirds that could be primarily attributed to atmospheric deposition. Our results indicated that songbirds at coastal sites averaged the highest mean blood Hg levels. Specifically, high Hg levels at coastal sites were found primarily in Saltmarsh Sparrow, Nelson’s Sparrow (Ammodramus nelsoni), and Seaside Sparrow (Ammodramus maritimus). Pairwise comparisons among coastal sparrow species indicated that Saltmarsh Sparrow mean blood Hg levels were significantly higher than Nelson’s Biodiversity Research Institute

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Sparrow (p < 0.0001), but no other significant differences existed among that group. Elevated blood Hg levels in coastal sparrows are discussed in greater detail below in Case Study #3. High mean blood Hg levels detected in songbirds in NH, VT, Western and Northern ME are primarily due to extremely high levels found in Rusty Blackbirds (Euphagus carolinus) and this research is highlighted below in Case Study #4. The overall mean blood Hg of songbirds sampled in Southwest VA along the Holston River is relatively low; however, maximum levels detected for certain species were very high (Figure 14). In particular, Indigo Buntings (Passerina cyanea) in this region had the highest mean blood Hg concentration of 0.28 ± 0.50 ppm (N = 10) and a maximum level of 1.67 ppm. During the breeding season, Indigo Buntings feed on small spiders and insects, such as caterpillars, beetles, and grasshoppers (Payne 2006). Songbirds that prey on higher trophic level invertebrates, such as spiders, increase their risk of Hg exposure and biomagnification. Cristol et al. (2008) analyzed spiders from this region and found that 49 ± 21% of their total Hg body burden was in the highly available form, MeHg, which is readily absorbed into the blood. Spiders in the riparian zone are potentially exposed to MeHg in the aquatic system if they feed on emergent aquatic insects. However, more research is necessary to determine whether predatory invertebrates represent a direct pathway for Hg to move from the aquatic food web into the terrestrial food web. Songbirds sampled within the Adirondack Park, NY region with the highest mean and maximum blood Hg levels, including Yellow Palm Warbler (Dendroica palmarum) ( = 0.57 ± 0.41 ppm, max = 1.49 ppm), Traill’s Flycatcher (Empidonax traillii) ( = 0.36 ± 0.26 ppm, max = 0.71 ppm), and Lincoln’s Sparrow (Melospiza lincolnii) ( = 0.19 ± 0.19 ppm, max = 0.66 ppm), were sampled in bog wetlands (Spring Pond Bog and Massawepie Mire) (Figure 15). Bog soils are low in dissolved oxygen and nutrients and are highly acidic; therefore, Hg is easily converted to MeHg in bog habitat. Yu et al. (2010) found that Sphagnum moss mats were prime locations for MeHg production and accumulation in bog wetlands in the Adirondack region. They proposed that submerged sponge-like structures of the plant are colonized by microorganisms capable of methylating Hg, such as sulfate-reducing bacteria. Furthermore, Hg is readily sorbed by moss tissues and methylation is facilitated by the anaerobic conditions around underwater plant parts. Spiders collected at Spring Pond Bog and Massawepie Mire had elevated MeHg levels; 0.34 ± 0.11 ppm and 0.15 ± 0.09 ppm, respectively. Spiders make up only a small portion of the primarily insectivorous breeding season diet of Yellow Palm Warbler, Traill’s Flycatcher, and Lincoln’s Sparrow; however, it is likely that their primary prey, e.g., beetles, flies, moths, within the same area would also be prone to elevated MeHg levels. Yellow Palm Warblers and Lincoln’s Sparrows feed primarily on the ground on their breeding habitat and are therefore excellent bioindicators of Hg levels within the bog wetland food web. Biodiversity Research Institute

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Blood Hg Level (ppm, ww) American Goldfinch (N = 2) Slate-colored Junco (N = 1) Black-throated Green Warbler (N = 1) Carolina Chickadee (N = 1) Northern Parula (N = 1) No. Rough-winged Swallow (N = 2) Grasshopper Sparrow (N = 1) Black-throated Blue Warbler (N = 1) Hooded Warbler (N = 1) Cedar Waxwing (N = 5) Black-and-White Warbler (N = 1) Blue-winged Warbler (N = 1) Yellow-throated Vireo (N = 1) Ovenbird (N = 2) Scarlet Tanager (N = 1) Veery (N = 11) Worm-eating Warbler (N = 2) Common Grackle (N = 3) Eastern Tufted Titmouse (N = 1) American Robin (N = 5) Great Crested Flycatcher (N = 1) Eastern Phoebe (N = 2) White-breasted Nuthatch (N = 1) Northern Cardinal (N = 2) Song Sparrow (N = 75) Wood Thrush (N = 12) Yellow-throated Warbler (N = 2) Red-eyed Vireo (N = 6) Carolina Wren (N = 28) Acadian Flycatcher (N = 12) Louisiana Waterthrush (N = 7) Red-winged Blackbird (N = 16) Indigo Bunting (N = 10)

Blood Hg Level (ppm, ww) 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 Maximum Level Detected

Mean + SD

Songbird Species Sampled in Southwest VA

Figure 14. Mean plus standard deviation and maximum level detected of blood Hg concentrations in songbirds sampled in Southwest VA, 2005 to 2007.

1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 Maximum Level Detected

Mean + SD

Songbird Species Sampled in Adirondack Mts, NY

Figure 15. Mean plus standard deviation and maximum level detected of blood Hg concentrations in songbirds sampled in Adirondack Mts, NY region, 2006 and 2007.

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5.3.2.1 CASE STUDY #3 - SALTMARSH SPARROW (LANE ET AL. 2011) The Saltmarsh Sparrow has a limited range, occupying estuaries along the Atlantic Coast from Florida up to the southern coast of Maine where it overlaps with the Nelson’s Sparrow (Hodgman et al. 2002). They are obligate salt marsh passerines with more than 95% of their global population breeding in the northeastern United States. The US Fish and Wildlife Service (USFWS) consider them one of the highest priority species in the northeast region and Photo provided by BRI staff classified them as a “bird of conservation concern”. This designation results from the near endemic status of this species in the region, a lack of population trend data, and threats on their breeding and wintering grounds. Saltmarsh Sparrows spend their entire annual cycle in salt marsh habitats, thus, they are excellent indicators of Hg contamination for this habitat type. Lane et al. (2011) sampled Saltmarsh Sparrow blood from estuaries from Maine to New York. Results revealed that blood Hg levels were highest at Parker River NWR in coastal MA ( = 1.80 ± 0.14 ppm). Nonparametric pairwise comparisons indicated that coastal MA blood levels were significantly higher than all other sampling locations (Figure 16, P < 0.01). Blood Hg levels were lowest at coastal CT and ME sites and they were significantly lower than MA, NY, and RI blood levels (P < 0.0001). Research conducted by Lane and Evers (2007) suggested that Saltmarsh Sparrow reproduction may be impaired by higher blood Hg concentrations. Based on one year of limited nest monitoring, productivity parameters such as number of eggs hatching and fledging appeared to be significantly lower at Parker River NWR, MA compared to Rachel Carson NWR, ME. Adult female Saltmarsh Sparrow blood Hg concentration were positively correlated with their nestling’s blood Hg levels, indicating that health of their young are compromised at hatching due to the deleterious effects of mercury. The ground-foraging habits of Saltmarsh Sparrows put them at high risk to mercury exposure in contaminated environments. On Long Island, New York, Merriam (1979) found that the two most common insect orders in their diet were Diptera, ranging between 13% in June to 47% of all items in July (predominantly adults and larvae of Stratiomyidae) and Hemiptera, ranging between 4% in June to 37% in July (nymphs and adults of Miridae). Additionally, their breeding-season diet may be comprised of up to 15% amphipod matter (Merriam 1979). Our study found that Dipterans and Amphipods have elevated Hg levels at coastal ME and MA sites. This example highlights a direct Hg pathway through several Biodiversity Research Institute

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orders of the food web. Mud-dwelling amphipods accumulate Hg while feeding on contaminated detritus in the soil and pass it to Saltmarsh Sparrows. Furthermore, it is passed to their nestlings thereby potentially reducing fledging success. 4.0

Blood Hg (ppm), ww

3.5

Maximum Level Detected Mean + SD

3.0 2.5 2.0 1.5 1.0 0.5 0.0 Coastal CT (N = 32)

Coastal NY (N = 27)

Coastal RI (N = 55)

Coastal ME (N = 220)

Coastal MA (N = 145)

Saltmarsh Sparrow Sampling Regions

Figure 16. Mean plus standard deviation and maximum level detected of blood Hg in Saltmarsh Sparrows sampled in coastal New England and Long Island, NY, 2000 to 2007.

5.3.2.2 CASE STUDY #4 - RUSTY BLACKBIRD (EDMONDS ET AL. 2010) Rusty Blackbirds breed in boreal bogs, marshes, ponds, and swamps of Alaska, Canada and northeastern US and winters in the wooded wetlands of the southeast-central US. Their populations have declined by an estimated 90% over the last 100 years and continue to decline at a significant rate of 13% per year (Sauer et al. 2008, Greenberg and Droege 1999). These losses are likely attributable to factors resulting in habitat loss and degradation, such as logging, development, drying of wetlands due to climate change, and increases in environmental contaminants. One such contaminant is mercury; the accumulation of which has been shown to have negative effects on the reproductive success of a closely related blackbird, Common Grackle (Quiscalus quiscula) (Finley et al. 1979, Heinz et al. 2009). Rusty Blackbirds may be at even greater risk to Hg exposure than other blackbird species because of their dietary preference for higher level trophic items, such as small fish and aquatic Biodiversity Research Institute

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invertebrates (Avery 1995). Additionally, habitat type plays a critical role in Hg exposure and recent research suggests that Rusty Blackbird breeding habitat is characterized by high levels of dissolved organic carbon and low pH, which have both been correlated with increased methylation, bioavailability, and retention of Hg (Scheuhammer 1991, O’Driscoll et al. 2005, 2006, Harding et al. 2006). In order to assess whether these factors resulted in high uptake of Hg by these declining populations, Edmonds et al. (2010) sampled Rusty Blackbirds in five regions across their range. Results indicated that geographic and seasonal differences in Hg concentrations existed among these regions. The blood Hg levels in birds sampled on the breeding range were significantly higher than those sampled on the wintering range. Of all the regions, the Northeast (Acadian Forests region) breeding region samples exhibited the highest Hg concentrations with levels 3× to 7× greater than any other region. Overall mean percent MeHg of THg was 98 ± 2% (N = 5) in blood and 97 ± 0.3% (N = 5) in feathers. Within New England, BRI sampled 93 Rusty Blackbirds between 2004 and 2010. Overall mean blood Hg concentration was 0.66 ± 0.41 ppm. The highest blood Hg level (2.05 ppm) was sampled in NH (Figure 17). The direct effects of elevated Hg concentrations on Rusty Blackbird populations are unclear. Reduced hatching success has been observed when THg levels in feathers were between 5 and 40 ppm, ww (Burger and Gochfeld 1997). Over 95% of the Acadian forest feather samples in Edmond et al.’s (2010) study exceeded this upper limit; however, Powell (2008) reported high nesting success of Rusty Blackbirds within this range. Feather sample results suggested that Rusty Blackbirds accrued much of their Hg burden on the breeding grounds. Blood level results, which indicate exposure from food consumed during the previous few days or weeks, also indicated that birds were exposed to the highest amounts of Hg while on the breeding grounds, particularly in the Northeast (Evers et al. 2005). Further research will be necessary to uncover potential links between elevated blood Hg concentrations and hatching success and survival rates of this species. Rusty Blackbird populations have suffered long-term declines over the last 100 years with an alarming acceleration in recent decades and these trends warrant immediate attention from conservation biologists and policy makers.

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Blood Hg Level (ppm, ww)

2.5 2.0

Maximum Level Detected Mean + SD

1.5 1.0 0.5 0.0

Rusty Blackbird Sampling Areas

Figure 17. Regional mean plus standard deviation and maximum level detected of blood Hg concentrations detected in Rusty Blackbirds in New England, 2007 to 2010. 5.3.3 MERCURY EXPOSURE BY FORAGING GUILD Foraging guild is an important factor when assessing risk of Hg exposure in songbirds. Evers et al. (2005) ranked Hg exposure risk in avian foraging guilds from lowest to greatest as terrestrial herbivores, aquatic herbivores, terrestrial insectivores, benthivore-bivalves, benthivore-macroinvertebrates, small piscivores, and large piscivores. Piscivorous birds have long been used as indicators of MeHg availability (e.g., Fimreite et al. 1974; Barr 1986; Scheuhammer 1987; Wolfe et al. 1998; Rumbold et al. 2001; Henny et al. 2002; Evers et al. 2003); however, our findings and other research (Wolfe and Norman 1998; Gerrard and St. Louis 2001; Adair et al. 2003) reveal that insectivorous birds are also useful gauges of Hg exposure within terrestrial habitats. In order to determine which feeding habits increased risk of Hg exposure, we compared mean blood Hg levels of sampled birds among the following foraging guilds (De Graaf et al. 1985): *Note: See Appendix A for latin names of songbirds in the following list. Frugivore Air/Upper-Canopy Cedar Waxwing Omnivore Upper-Canopy Rose-breasted Grosbeak

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Insectivore Air/Lower-Canopy American Redstart Hooded Warbler Omnivore/Vermivore Ground/LowerCanopy American Robin Page 37

Insectivore Upper-Canopy Cerulean Warbler Northern Parula Black-throated Green Warbler Blackpoll Warbler Scarlet Tanager Red-eyed Vireo Yellow-throated Vireo

Omnivore Ground/Lower-Canopy American Goldfinch Veery Brown Thrasher Gray Catbird Swainson's Thrush Bicknell's Thrush Song Sparrow

Insectivore Bark Black-and-White Warbler Brown Creeper White-breasted Nuthatch Red-breasted Nuthatch

Insectivore Air Northern Rough-winged Swallow Eastern Kingbird Yellow-bellied Flycatcher Barn Swallow Least Flycatcher Great Crested Flycatcher Eastern Phoebe Cliff Swallow Tree Swallow Acadian Flycatcher Traill's Flycatcher Eastern Wood-Pewee

Insectivore Lower-Canopy White-eyed Vireo Prairie Warbler Black-throated Blue Warbler Boreal Chickadee Blue-winged Warbler Blue-headed Vireo Tufted Titmouse Black-capped Chickadee Magnolia Warbler Myrtle Warbler House Wren Common Yellowthroat Carolina Wren Omnivore Lower-Canopy Carolina Chickadee Indigo Bunting

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Insectivore Bark/Upper-Canopy Yellow-throated Warbler Insectivore Freshwater Shoreline Louisiana Waterthrush Northern Waterthrush Insectivore Ground Mourning Warbler Ovenbird Winter Wren Worm-eating Warbler Yellow Palm Warbler Rusty Blackbird

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Insectivore Marsh Marsh Wren Omnivore Ground White-throated Sparrow Savannah Sparrow Bobolink Slate-colored Junco Grasshopper Sparrow Hermit Thrush Eastern Towhee Wood Thrush Chipping Sparrow Common Grackle Lincoln's Sparrow Northern Cardinal Swamp Sparrow Red-winged Blackbird Seaside Sparrow Nelson's Sparrow Saltmarsh Sparrow

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Blood Hg Level (ppm, ww)

4.0 3.5

Maximum Level Detected Mean + SD

3.0 2.5 2.0 1.5 1.0 0.5 0.0

Songbird Foraging Guilds

Figure 18. Mean blood Hg level (ppm) by songbird foraging guild as defined by De Graaf et al. (1985). Among songbirds sampled in New England and the Mid-Atlantic States, insectivores and ground-feeding species, particularly those feeding in wetland habitats, had the greatest blood Hg levels (Figure 18). As discussed previously, Saltmarsh, Nelson’s and Seaside Sparrows (omnivore ground), Rusty Blackbird (insectivore ground), and Yellow Palm Warbler (Dendroica palmarum) (insectivore ground) exhibited high blood Hg levels and largely drove the trends observed in those guilds (Figures 19 & 20). Red-winged Blackbirds (N = 40) are omnivore ground feeders with moderately high Hg blood levels; they were primarily sampled in southern NY (Bashakill WMA: x = 0.23 ± 0.09ppm, N = 12; Bog Brook WMA: x = 0.25 ± 0.25 ppm, N = 2; and Mohonk Preserve: x = 0.08 ppm, N = 1), Southwest VA (two locations on Holston River: x = 0.20 ± 0.29 ppm, N = 16), and coastal ME (Crane Pond WMA: x = 0.39 ± 0.30 ppm, N = 7).

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Blood Hg Level (ppm, ww)

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

Maximum Level Detected Mean + SD

Omnivore Ground Foraging Guild

Blood Hg Level (ppm, ww)

Figure 19. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “omnivore ground” foraging guild species sampled in New England and Mid-Atlantic States, 2000 to 2007. 2.5 2

Maximum Level Detected Mean + SD

1.5 1 0.5 0

Insectivore Ground Foraging Guild

Figure 20. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore ground” foraging guild species sampled in New England and the Mid-Atlantic States, 2004 to 2010. Biodiversity Research Institute

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In upland habitats, Wood Thrushes were omnivore ground feeders that frequently exhibited high blood Hg levels. BRI collected Wood Thrush blood and soil samples from the Institute for Ecosystem Studies in Millbrook, NY. We compared blood Hg levels in the ground-foraging wood thrush with soil Hg and Ca concentrations to determine correlations between these variables. 5.3.3.1 CASE STUDY # 5 - RELATIONSHIP BETWEEN SOIL Hg AND A GROUND-FORAGING SONGBIRD: THE WOOD THRUSH The Wood Thrush is a songbird of the eastern US found in hardwood forests consisting of a high canopy, dense understory, and thick leaf litter layer. While it is generally considered a common species, it has suffered recent significant range wide declines of –1.7% per year across its range (Sauer et al. 2008). In New England, it is declining at –2 to –3% per year and up to –4.4% per year in the Photo by Steve Maslowski/USFWS Adirondack Mts, NY (Sauer et al. 2008). The 2nd New York Breeding Bird Atlas documented a –7.0% decline in Wood Thrush occupancy between 1985 and 2005; the majority of those declines occurred in the Adirondack Mts (Hames and Lowe 2008). They attributed winter habitat loss, over-winter mortality, acid rain, and mercury deposition as the mostly likely contributors to the loss of wood thrush populations. Hames et al. (2002) found that the probability of occupancy of a site by breeding Wood Thrushes decreased with increasing acid rain deposition, which was further compounded in low pH soils. Hames et al. (2006) found that soil pH was highly significantly and positively related to the abundance of calcium-rich invertebrates, i.e., myriapods, isopods, and slugs. They also found that soil calcium was proportional to soil pH and they postulated that absences of breeding wood thrushes was related to the decreased availability of calcium-rich invertebrate prey items associated with acidified soils. We examined the relationship between soil Hg and available Ca in soils with blood Hg levels in Wood Thrushes during the breeding season. We measured multiple soil characteristics of organic and mineral layer soil samples collected at the Institute for Ecosystem Studies in Millbrook, NY (see soil section for complete analysis). We measured blood Hg levels of Wood Thrushes (N = 5) occupying the same soil sampling locations. Wood Thrush blood Hg levels were highest at sites with high soil Hg and low exchangeable

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Ca levels. There was an inverse relationship between blood Hg and exchangeable Ca levels and a positive relationship between blood Hg and soil Hg levels (Figures 21 & 22).

WOTH Blood Hg (µg/g), ww

0.20

Organic Mineral

0.15

0.10

0.05

0.00 80

100

120

140

160

180

Soil Layer Hg (µg/kg), ww

Figure 21. Relationship between the amount of exchangeable calcium in the organic and mineral soil layer and Wood Thrush (N = 6) blood Hg concentrations. Small sample size precludes statistical reliability; however, preliminary analysis indicates: organic soil: R2= 0.55; mineral soil layer: R2 = – 0.67). Mineral

WOTH Blood Hg (ppm), ww

0.15

Organic 0.10

0.05

0.00 0

2

4

6

8

10

12

Soil Exchangeable Ca

Figure 22. The relationship between the amount of exchangeable Ca in the organic and mineral soil layers and blood Hg concentrations of Wood Thrushes (N = 6). Small sample size precludes statistical reliability; however, preliminary analysis indicates: organic soil layer: R2 = – 0.45; mineral soil layer: R2 = – 0.67. Biodiversity Research Institute

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The effects of calcium deficiency on birds can be species and even population specific (Mand and Tilgar 2003). Subtle differences in food web pathways for MeHg biomagnification and transfer can also create multiple-fold differences in blood Hg exposure in sibling species within the same areas (Shriver et al. 2006). Since the Wood Thrush feeds primarily on the forest floor by moving leaf litter to locate prey items (Holmes and Robinson 1988), the pathway of MeHg through its prey is likely connected with the organic soil. This analysis indicates that the Wood Thrush is a valuable choice as an indicator species when linking abiotic and biotic compartments of Hg with Ca. The omnivore lower-canopy guild was comprised mostly of Indigo Buntings (N = 11) discussed above in the regional comparisons section. The insectivore air foraging guild is limited to flycatchers (Tyrannidae) and swallows (Hirundinidae) (Figure 23). Tyrannidae species had the highest blood Hg levels and are discussed in greater detail below in the family comparisons section. Cliff Swallows (Petrochelidon pyrrhonota) were sampled in riparian habitat within western and northern Maine ( = 0.21 ± 0.09 ppm; max = 0.47 ppm). They are diurnal foragers and group feed on swarms of insects; the types of insects taken tend to reflect local availability and vary widely. Barn Swallows (Hirundo rustica) and Tree Swallows (Tachycineta bicolor) have a similar diet to the Cliff Swallow; common food items taken by these species include Homopterans, Dipterans, Hymenopterans, Coleopterans, Ephemeropterans, Hemipterans, Lepidopterans, Orthopterans, and Odonates (Robertson et al. 1992, Brown and Brown 1999). Swallow species that forage over open water on emergent aquatic species are at increased risk of exposure to the MeHg that is prevalent in aquatic ecosystems of northeastern US. Omnivore ground/lower-canopy feeders ranged widely in their blood Hg levels; species with the highest levels included Bicknell’s Thrush (Catharus bicknelli) and Song Sparrow (Melospiza melodia) (Figure 24). Bicknell’s Thrush is exposed to high Hg levels in their montane habitat and is discussed in greater detail in Case Study #6. Song Sparrows were sampled in 11 regions in relatively low numbers, with the exception of southwest VA (N = 75) where mean blood Hg was 0.13 ± 0.09 ppm and the maximum level detected was 0.37 ppm. Song Sparrows tend to occupy shrubby areas along streams, marsh, or coastline but will utilize a wide range of habitats (Arcese et al. 2002). Their breeding season diet is primarily comprised of animal matter, of which they feed on a wide variety of taxa that tends to vary by ecoregion (Aldrich 1984). Their diet and foraging locations make Song Sparrows excellent bioindicators of Hg exposure risk in scrub-shrub zones adjacent to aquatic habitats.

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Blood Hg Level (ppm, ww)

1.4 1.2 1

Maximum Level Detected Mean + SD

0.8 0.6 0.4 0.2 0

Insectivore Air Foraging Guild

Figure 23. Mean plus standard deviation and maximum level detected of blood Hg concentrations among “insectivore air” foraging guild species sampled in New England and Mid-Atlantic States, 2005 to 2007.

Blood Hg Level (pm, ww)

1.0 0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2 0.0

Omnivore Ground/Lower-Canopy

Figure 24. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “omnivore ground/lower-canopy” foraging guild species sampled in New England and Mid-Atlantic States, 1999 to 2007. Biodiversity Research Institute

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Blood Hg Level (ppm, ww)

Insectivore upper-canopy feeders tended to have low blood Hg levels with the exception of several Red-eyed Vireo (Vireo olivaceus) and Yellow-throated Vireo (Setophaga dominica) individuals (Figure 25). Red-eyed Vireo maximum blood Hg levels ranged widely by sampling location; the lowest maximum level detected was 0.03 ppm at George L. Darey Housatonic Valley WMA in western MA and the highest was 0.51 ppm along the Holston River in southwest VA. High levels were also observed at: Witch Hole Pond in Acadia National Park in coastal ME (0.43 ppm); Elk Lake (0.35 ppm), Dome Island, Lake George (0.27 ppm), and Arbutus Lake (0.25 ppm) in the Adirondack Mts, NY; a residential neighborhood in Standish, ME (0.30 ppm); and Tott’s Gap (0.29 ppm) in PA . Two Yellowthroated Vireos were sampled; one sampled along the Holston River in Southwest VA had relatively low blood Hg (0.07 ppm) and the other sampled at Bashakill WMA in southern NY had a high blood Hg of 0.72 ppm. Major food items eaten by these species include Lepidopterans, Dipterans, Coleopterans, Hemipterans, Homopterans and Hymenopterans; less frequently they consume Orthopterans, Odonates, Arachnids, and Mollusks (Cimprich et al. 2000). High blood Hg levels observed in individual vireos likely represent differences in site contamination but also differences in foraging locations and food items eaten by individuals. Individuals that consume greater quantities of spiders and other carnivorous invertebrates are at greater risk of MeHg exposure. 1.0 0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2 0.0

Insectivore Upper-Canopy

Figure 25. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore upper-canopy” foraging guild species sampled in New England and the Mid-Atlantic States, 1999 to 2010. Biodiversity Research Institute

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The Northern and Louisiana Waterthrushes are closely related warbler species with overlapping ranges and habitats and they fill a unique role in the eastern US as “freshwater shoreline foragers” (De Graaf et al. 1985). The Northern Waterthrush (Parkesia noveboracensis) breeds from Alaska and much of Canada south to the northern U.S, and the Louisiana Waterthrush (Parkesia motacilla) breeds from Minnesota, southern Ontario and central New England south to Texas and Georgia. Both can be found in mixed forests, but Northern Waterthrush is typically associated with coniferous woods containing swamps, bogs, lakes, and willow/alder-bordered rivers. In contrast, Louisiana Waterthrush habitat is more often deciduous cover near swift-moving brooks on hillsides, river swamps, and along sluggish streams. Both species’ diets include a high biomass of aquatic prey (Craig 1984). Both forage at water’s edge for the following insect families: Chironomids, Coleopterans, Diplopods, Ephemeropterans, Hemipterans, Neuropterans, Plecopterans, Stratiomyiids, Tipulids, and Trichopterans (Robinson 1995). Additional prey includes snails and other mollusks, arachnids, amphibians, and small fish. These prey items likely explain their relatively high Hg body burdens (Figure 26). The effects these body burdens may have on Louisiana Waterthrush are of particular interest because it is a neotropical migrant of high conservation concern (Rich et al. 2004). Indeed, comparisons of New York’s Breeding Bird Atlas data for the first (1980-1985) and second (2000-2004) periods indicate a substantial – 21% loss of breeding records (Rosenbeg 2008). Mulvihill et al. (2008) compared breeding Louisiana Waterthrush territories along an acidified stream and a circumneutral stream and found that birds along the acidified streams were generally young, inexperienced birds and that they exhibited lower breeding density, later first laying dates, lower site fidelity, and traveled further when foraging for food. Stream acidity did not appear to have an effect on nest success or fecundity; however, the number of young fledged was twice as high on circumneutral streams. Methylmercury availability and its effects on insectivorous passerines require further investigation, but based on limited data, Louisiana and Northern Waterthrushes may be at greatest risk among that feeding guild in riverine systems.

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0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2

Louisiana Waterthrush

Southern NY (N = 5)

Northern ME (N = 1)

Southern NY (N = 2)

Southwest VA (N = 7)

Central/Western NY (N = 3)

Catskill Mts, NY (N = 4)

0.0 PA (N = 4)

Blood Hg (ppm), ww

1.0

Northern Waterthrush

Figure 26. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Louisiana Waterthrush and Northern Waterthrush sampled in New England and Mid-Atlantic States, 2005 to 2007. Elevated blood Hg levels of insectivore lower-canopy feeding species were primarily observed in Carolina Wrens (Thryothorus ludovicianus) and several warblers (Figure 27). These included: Common Yellowthroats (Geothlypis trichas) at Ferd’s Bog (0.31 ppm) and Spring Pond Bog (0.33 ppm) in the Adirondack Mts, NY, Crane Pond WMA (0.24 ppm) in coastal MA, and Great Swamp WMA (0.41 ppm) in southern NY; Magnolia Warbler (Dendroica magnolia)at Arbutus Lake (0.22 ppm) in the Adirondack Mts, NY; and Myrtle Warbler (Dendroica coronata) at Spring Pond Bog (0.32 ppm) in the Adirondacks Mts, NY and along the East Kennebago River (0.16 ppm) in western ME. Insectivore bark/uppercanopy foraging guild was comprised of two Yellow-throated Warblers (Setophaga dominica) sampled along the Holston River in Southwest VA ( = 0.26 ± 0.20 ppm; max = 0.41 ppm). Insectivore marsh foraging guild consisted of two Marsh Wrens (Cistothorus palustris) sampled at McKinney NWR in coastal CT ( = 0.25 ± 0.003 ppm). Marsh Wrens feed primarily on insects and spiders at or near the surface of the water in freshwater, saltwater, and brackish marshes (Kroodsma and Verner 1997). In the New England and Mid-Atlantic Coast, Marsh Wrens declined at a significant annual rate of -2.9% between 1966 and 2009. Although our small sample size limits speculation on whether Marsh Wren populations are being affected by high levels of Hg, further research to determine the effects of blood Hg on the reproductive success of Marsh Wrens in this region is warranted given the nature of their diet and habitat. Biodiversity Research Institute

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Blood Hg (ppm), ww

1.0 0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2 0.0

Insectivore Lower-Canopy

Figure 27. Mean plus standard deviation and maximum level detected of blood Hg concentrations in “insectivore lower-canopy” foraging guild species sampled in New England and Mid-Atlantic States, 2004 to 2007. Blood Hg levels in the remaining foraging guilds were generally low. The highest levels observed in insectivore bark foraging guild was in a White-breasted Nuthatch (Sitta carolinensis) (0.24 ppm) sampled along the Holston River in Southwest VA and a Redbreasted Nuthatch (Sitta canadensis) (0.14 ppm) sampled in Spring Pond Bog in the Adirondack Mts, NY. The omnivore/vermivore ground/lower-canopy foraging guild is comprised solely of the American Robin (Turdis migratorius), whose maximum blood Hg levels were found along the Holston River in southwest VA (0.19 ppm) and in a residential neighborhood in southern Maine (0.15 ppm). The insectivore air/lower canopy foraging guild consisted of American Redstart (Setophaga ruticilla) and Hooded Warbler (Wilsonia citrina). American Redstart sample size and blood Hg levels were low; however, one individual sampled in Black Rock Forest in Southern NY had a blood Hg level of 0.19 ppm. Likewise, Hooded Warbler sample sizes were low and so were blood Hg levels; however, one individual sampled in Allegany State Park in Central/Western NY had a blood Hg level of 0.18 ppm. Blood Hg levels were negligible in the last two foraging guilds, frugivore upper-canopy and omnivore upper-canopy; however, sample sizes were very small. Frugivore upper-canopy foraging guild consisted of Cedar Waxwings sampled along the

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Holston River in Southwest VA and one Rose-breasted Grosbeak sampled in Devil’s Tombstone in the Catskill Mts, NY made up the omnivore upper-canopy foraging guild. 5.3.4 MERCURY EXPOSURE BY FAMILY

Mean Blood Hg (ppm, ww)

Regional and foraging guild analyses indicated that many of the species with the highest blood Hg levels were closely-related, e.g., coastal sparrows and Rusty and Red-winged Blackbirds. These results warranted further examination of family groupings to determine whether certain genera were prone to Hg biomagnifications. Indeed, the Emberizidae and Icteridae families had the highest means (Figure 28), with members associated with wetlands exhibiting greater levels than their upland relatives. For example, the coastal sparrows and the Swamp Sparrow (Melospiza georgiana) ( = 0.43 ± 0.36) had the highest levels among the Emberizids (Appendix B). Similar patterns are apparent in the Icteridae, Parulidae, and Troglodytidae family groups (Appendix B). 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

Maximum Level Detected Mean + SD

Figure 28. Mean plus standard deviation and maximum level detected of blood Hg concentrations among songbird families sampled in New England and Mid-Atlantic States, 1999 to 2010. Tyrannidae, the flycatchers, had the third highest mean Hg blood levels among the family groups. They are part of the insectivorous air foraging guild and feed on a wide range of invertebrate species. Two Eastern Wood-Pewees (Contopus virens) sampled near Great Swamp WMA in southern NY had the highest mean blood Hg levels (Figure 29). Traill’s Flycatchers (Willow/Alder flycatcher) in the Adirondack Mts, NY and Acadian Flycatchers along the Holston River in Southwest VA had the highest blood Hg levels among flycatchers in those sampling regions, = 0.36 ± 0.24 (N = 4) and = 0.29 ± 0.13 (N = 12), respectively. Traill’s Flycatchers are generally found in shrubby wetlands and Acadian Flycatcher Biodiversity Research Institute

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Blood Hg Level (ppm, ww)

(Empidonax virescens) habitat is riparian forests. Due to their aquatic ecosystem associations, it is not surprising to find elevated blood Hg levels, particularly within known mercury hotspots. 1.4 1.2

Maximum Species Level Detected

1.0

Mean + SD

0.8 0.6 0.4 0.2 0.0

Tyrannidae

Figure 29. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Tyrannidae species sampled in New England and Mid-Atlantic States, 2005 to 2007. The Eastern Wood-Pewee, on the other hand, is a relatively common songbird associated with open forests that forages in the middle section of the understory up to the lower canopy. Our sample size was very low, however, the blood Hg levels in the individuals we sampled were very high indicating that Eastern Wood-Pewees are capable of accumulating deleterious Hg concentrations from its diet. Typically, their diets consists of small, flying insects, including Dipterans, Homopterans, Lepidopterans, Hymenopterans, Coleopterans, Orthopterans, Plecopterans, and Ephemopterans (McCarty 1996). The two individuals we sampled were in Great Swamp WMA, which is a red maple swamp in Southern NY. While the Eastern Wood-Pewee is not listed as a species of special concern anywhere, its populations are decreasing across its range at a significant rate of –1.7% per year (Sauer et al. 2008). Within our study area, annual significant declines approach –3% to –4% in sections of New York and New England and up to –7.4% in the Blue Ridge Mountains of Virginia (Sauer et al. 2008). The 2nd New York Breeding Bird Atlas noted that while the species was still a common and widespread bird, it was disappearing from sites with marginal habitat which is generally where populations changes are first detected (McGowan 2008). It listed potential causes for this decline as maturation of forests in the northeast and changes on the wintering grounds in northern South America. Biodiversity Research Institute

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Hg contamination may be a co-stressor to species facing population declines due to habitat loss and degradation. The Great Swamp WMA provides much-needed hardwood swamp habitat for a variety of songbird species; however, two types of invertebrate prey, ground beetles (Carabidae) and Long-jawed Orb Weavers (Tetragnathidae), sampled at this site had elevated total MeHg levels: = 0.08 ppm, dw (N = 2) and = 0.10 ppm, dw (N = 2), respectively. Additional samples are necessary to draw a clear connection between available Hg in prey and blood Hg levels in songbirds at this site, but it should be noted that three songbird species sampled here (Common Yellowthroat, Song Sparrow, and Wood Thrush) exhibited blood Hg levels that were twice as high as the overall species’ mean blood level detected across their sampling range. The degree of Hg exposure among species is correlated with trophic position and MeHg availability (Evers et al. 2005). For closely-related species that occupy similar trophic positions, there are several factors that determine each species’ degree of MeHg exposure, including: geographic area, foraging guild, and habitat type. Members of the thrush family, Turdidae, illustrate how differences in habitat and microhabitat can affect blood Hg levels among closely-related species occupying similar foraging guilds within the same geographic area. In the case of the Bicknell’s Thrush, we see the additive effects. 5.3.4.1 SONGBIRD CASE STUDY #6 - BICKNELL’S THRUSH The Bicknell’s Thrush is relegated to breeding in subalpine areas of conifer-dominated forests with elevation thresholds that are latitudinally controlled (Lambert et al. 2005); in the U.S., lowest elevations occupied are in northern Maine at 750m, while in the southernmost extent of its range in the Catskill Mountains the Bicknell’s Thrush generally breeds on mountains 1,100 m or higher (Rimmer et al. 2001). Montane habitats in the Northeast are subjected 2-5× higher Hg input than surrounding low elevation habitats (Miller et al. 2005). Cloud and fog water can directly deposit pollutants onto the high elevation landscapes they come into contact with, and furthermore, the topographical features of mountains enhance precipitation rates (as indicated by Rimmer et al. 2005). These factors appear to contribute to high levels of Hg deposition. Additionally, the thin, sandy mountaintop soils in the northeastern US have low calcite levels, and thus, low buffering capacity from acidic input, such as sulfuric and nitric acids, resulting in lower soil pH (Driscoll et al. 2001). Therefore, these soils are often more acidic than lower elevation soils containing highly buffered, thick organic soil layers (Bernard et al. 2009). As we discussed previously in the soil section, acidified soils can have multiple ramifications on songbirds. The ability of Hg to methylate in dry soils are unclear, but Rimmer et al.’s (2010) study of a montane food webs documented an increasing trend in MeHg levels with increasing trophic level. Based on these findings, it appears that high elevation forests Biodiversity Research Institute

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species, such as the Bicknell’s Thrush, should have proportionally higher Hg levels than its relatives occupying similar niches in low elevation forests. Indeed, we compared thrush blood Hg levels and found that Bicknell’s Thrush had significantly higher levels than all other thrush species (P ≤ 0.05) (Figure 30). Rimmer et al. (2005) stated that Bicknell’s Thrush was a useful bioindicator of MeHg in high-elevation fir-dominated forests. We focused on sampling Bicknell’s Thrush in montane habitats throughout the northeastern US to determine geographic differences in blood levels (Figure 31), but we found no significant differences.

Blood Hg Level (ppm, ww)

1.0 Maximum Species Level Detected 0.8

Mean + SD

0.6 0.4 0.2 0.0

Turdidae

Figure 30. Mean blood Hg concentration in Turdidae family species sampled in New England and Mid-Atlantic States, 1999 – 2008. Bicknell’s Thrush blood Hg levels were significantly higher than all other thrush species (P ≤ 0.05). The habitat of the Bicknell’s Thrush places it at higher risk of Hg exposure than other thrush species; however, the threat of Hg exposure in those species is no less significant. Among thrushes found in the northeastern US, the Eastern Bluebird (Sialia sialis) likely has the lowest Hg exposure risk due to a largely frugivore diet and old field habitat. The remaining thrushes are generally categorized as ground-foraging omnivores, although some also feed in the lower canopy. Holmes and Robinson (1988) found that in northern hardwood forests where habitat and range overlapped for several thrush species, they partitioned available resources by occupying different macrohabitat, microhabitat, preyattack methods, and diet. Wood Thrush, Veery (Catharus fuscescens) , Swainson’s Thrush Biodiversity Research Institute

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Blood Hg Level (ppm, ww)

(Catharus ustulatus) , and Hermit Thrush (Catharus guttatus) fed frequently on the ground; however, Wood Thrush fed almost exclusively on the ground while the others also fed in the sapling, subcanopy, and, occasionally, the canopy. The Swainson’s Thrush utilized the canopy most often and focused 10% of its prey attacks in that foliage stratum. The majority of our Swainson’s Thrush samples were obtained at many of the same sites as the Bicknell’s Thrush samples, yet the Swainson’s Thrush had significantly lower blood Hg levels. Typically, Hg concentrations in the leaf litter are higher than levels in the live foliage (Rimmer et al. 2010). If indeed certain thrush species or individuals spend more time foraging in the live foliage, they may be exposed to less Hg than thrushes that feed almost exclusively in the leaf litter layer, such as the Wood Thrush and Bicknell’s Thrush. These characteristics make Bicknell’s Thrush an excellent indicator species of available Hg in the leaf litter layer for high elevation sites, whereas the Wood Thrush appears to be an excellent indicator in low elevation forest sites, particularly those adjacent to rivers and wetlands. 1.0 0.8

Maximum Level Detected Mean + SD

0.6 0.4 0.2 0.0

Bicknell's Thrush Sampling Areas

Figure 31. Regional means plus standard deviations and maximum levels detected of blood Hg concentrations Bicknell’s Thrush sampled in New England and New York, 1999 – 2007. 5.3.5 BLOOD MERCURY CONCENTRATIONS AND REPRODUCTIVE SUCCESS Survival, reproduction, immune response, song, and endocrine function are all aspects of songbird ecology that may be adversely affected by elevated blood Hg levels (Hallinger et al. 2010, Brasso and Cristol 2008, Hawley et al. 2009, and Wada et al. 2009). Brasso and Cristol (2008) studied Tree Swallows along the South River in Virginia and found that second-year birds along a polluted section of river produced fewer chicks than those in the uncontaminated reference area. There was a significant and positive relationship between Biodiversity Research Institute

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female tree swallow blood mercury levels and the average mercury levels of eggs (Brasso et al. 2010). Adult female birds depurate some of their Hg body burden during the egglaying process as it is deposited into the albumen, shell, and yolk (Kennamer et al. 2005). The percentage of Tree Swallow eggs that survived to produce a fledgling was significantly lower at the contaminated site compared to the reference site (Brasso and Cristol 2008). However, they were unable to predict nest success based on the female’s blood Hg concentration. Recently, BRI recently conducted research to assess reproductive success of a terrestrial forest invertivore, the Carolina Wren (Thryothorus ludovicianus) and successfully developed effects concentrations based on their findings, which are highlighted in Case Study # 7. 5.3.5.1 SONGBIRD CASE STUDY # 7 - CAROLINA WREN (JACKSON ET AL. 2011) Carolina Wren nest boxes were monitored for nest success along known contaminated sections of the South River and North Fork Holston River in Virginia and along several nearby uncontaminated reference rivers. Carolina Wrens near the contaminated sites showed blood Hg levels that were 7 to 10 times higher than reference site birds. Additionally, those individuals at contaminated sites had 34% reduced reproductive success compared to those at reference sites. Female blood Hg concentration was a good predictor of overall nest Photo provided by BRI staff success; birds with higher Hg body burdens were less likely to successfully fledge young. Jackson et al. (2011) documents Hg effects concentrations in blood, feathers and eggs for Carolina Wrens that corresponds with range of reduced nest success (Table 1). According to the 10% nest reduction effects concentration, it appears that 12 of the 82 songbird species we sampled had individuals with blood Hg levels that put them at risk of reduced nest success (Figure 32).

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Table 1. Carolina Wren blood, feather, and egg Hg effects concentrations associated with MCestimate-modeling reduction in nest success (adapted from Jackson et al. 2011). Mercury Risk Categories

Reduction in Nest Success

Blood Hg (ppm, ww)

Body Feather Hg (ppm, fw)

Tail Feather Hg (ppm, fw)

Egg Hg (ppm, ww)

Low

10%

0.7

2.4

3.0

0.11

Moderate

20%

1.2

3.4

4.7

0.20

High

30%

1.7

4.5

6.4

0.29

40%

2.1

5.3

7.7

0.36

50%

2.5

6.2

9.1

0.43

60%

2.9

7.1

10.4

0.50

70%

3.3

7.9

11.8

0.57

80%

3.8

9.0

13.5

0.66

90%

4.4

10.3

15.5

0.76

99%

5.6

12.8

19.5

0.97

Very High

Blood Hg Level (ppm, ww)

4.0 3.5 3.0

Maximum Species Level Detected Species Mean + Standard Deviation

2.5 2.0

- 30% reduced nest success

1.5

- 20%

1.0

- 10%

0.5 0.0

Figure 32. Songbird species sampled in New England and the Mid-Atlantic States between 1999 and 2010 with individuals whose blood Hg (ppm, ww) concentrations put them at risk of reduced nesting success. Risk categories associated with 10% (0.7 ppm), 20% (1.2 ppm), 30% (1.7 ppm) reduced nesting success are based on Jackson et al.’s (2011) Carolina Wren research. *Indicates neotropical migrant species. Biodiversity Research Institute

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5.4 CONCLUSIONS There are compelling reasons to be concerned about the effects of airborne pollutants on breeding songbirds in eastern forests. Much is already known about the effects of acidic deposition on northeastern landscapes and the depletion of available Ca in soil, but only recently has acidification also been implicated in increased MeHg availability. The distribution of Hg and the availability of MeHg are now well documented in the Northeast. Detection of this pattern was accomplished through a four-year study funded by the USDA Forest Service. BRI and their collaborators compiled and synthesized most of the publicly available mercury data in the Northeast into a series of 21 papers in a special issue of Ecotoxicology (Evers and Clair 2005). From this comprehensive review on how Hg is distributed across the landscape, three findings emerged that partly serve as a basis for this current investigation: (1) new findings indicate MeHg availability is more prevalent in terrestrial birds than previously considered (Evers et al. 2005); (2) birds in montane terrestrial habitats may be at risk (Rimmer et al. 2005), likely as a consequence of a higher rate of atmospheric deposition of wet and dry Hg than in lower elevation habitats (VanArsdale et al. 2005); and (3) there is a significant relationship between wet and dry Hg deposition models based on Miller et al. (2005) and on Bicknell’s Thrush blood Hg levels (Rimmer et al. 2005). The comprehensive sampling effort of songbirds discussed in this report revealed elevated blood Hg levels, and in some areas, above levels of concern. Patterns of blood Hg levels indicate that body size, habitat type, elevation, and geographic location are important variables to measure. Some species, such as the Saltmarsh Sparrow, Rusty Blackbird, and Louisiana Waterthrush appeared to bioaccumulate greater amounts of MeHg than other species and are experiencing declines in population size. As electric utilities are the major sources of atmospheric Hg in the U.S., results from this investigation provide important information to policy makers on the pervasiveness of Hg in the Northeast and how synergy with other stressors such as acidic deposition could have broad-scale impacts to bird populations and ecosystem health. If future efforts link emission sources from the Ohio River Valley with biological Hg hotspots in New England and Mid-Atlantic States, the need for implementation of the Mercury and Air Toxics Standards (MATS) Rule by the U.S. Environmental Protection Agency is even more compelling (U.S. EPA 2011). No individual point source in New England, New York, or New Jersey releases more than 500 pounds of Hg per year, while several sources in Pennsylvania and Ohio exceed this annual rate of release. Continued research could ultimately contribute to a framework for new national legislation to regulate Hg emissions and standardize monitoring efforts. Should the decline of songbirds truly signal a widespread and major disruption in how forests function in New England and the MidAtlantic region, then this effort is very timely to better define potential sources of declines in songbird populations. Biodiversity Research Institute

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6.0 BATS

6.1 STUDY AREA Bat capture and sampling occurred in multiple territory locations at 44 sites distributed across 7 New England and Mid-Atlantic States (Figure 33). 6.2 METHODS Single, double, and triple high mist nets were strung directly in front of ledge outcroppings, between trees along small access roads, or in the middle of rivers to funnel bats into nets. Using the assumption that bats fly to water for drinking and feeding purposes after leaving daytime roosts, roads that led towards water were chosen. Nets were set at dusk and monitored until at least 2300 hours; if bats were being captured, nets were left open until 0100 hours. All bats captured were identified to species, checked for reproductive status, sexed, and aged. Fur samples were cut from the back and abdomen collected with clean stainless steel scissors and collected into ziplock bags. Total mercury (THg) concentrations are reported as parts per million fresh weight (ppm, ww). The percent methylmercury (MeHg) present in bat fur is not known; however, Porcell (2004) found that 90% or greater of THg in raccoon hair was MeHg. All bats were released unharmed at the site. 6.3 RESULTS AND DISCUSSION 6.3.1 SPECIES MERCURY EXPOSURE We sampled 802 bats representing 13 species between 2006 and 2008. Adult fur Hg levels ranged from 0.69 ppm in a Red Bat (Lasiurus borealis) sampled in Monongahela National Forest in WV to 120.31 ppm in a Big Brown Bat (Eptesicus fuscus) sampled along the Little River in NH. Juvenile fur Hg levels ranged from 0.29 ppm in a Little Brown Bat (Myotis lucifugus) sampled along Middle River in VA to 18.83 ppm in a Little Brown Bat sampled in Biodiversity Research Institute

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Scarborough Marsh in coastal ME. Big Brown Bat ( = 17.78 ± 22.18 ppm), Southeastern Myotis (Myotis austroriparius) ( = 10.50 ± 9.33 ppm), Indiana Bat (Myotis sodalis) ( = 10.58 ± 5.07 ppm), and Evening Bat (Nycticeius humeralis) ( = 10.56 ± 7.99 ppm) had the highest mean fur Hg concentrations (Figure 34). Very few investigations have been conducted related to wild bats’ exposure to heavy metals in the environment. Baron et al. (1999) completed a risk assessment for aerial insectivorous wildlife on the Clinch River, TN (Oak Ridge Reservation). Using a model, they determined the dose levels for the NOAEL and LOAEL for little brown bats to be 0.11 and 0.56 ppm, respectively. Bats experiencing exposure equal or greater than the LOAEL were found to display impaired growth, reproduction, and offspring viability (Verschuuren et al. 1976). All of our Little Brown Bat samples, which ranged from 0.29 to 35.00 ppm, exceeded the NOAEL of 0.11 ppm and 90% had levels that exceeded the LOAEL of 0.56 ppm. Burton et al. (1977) found that mice with fur Hg concentrations of 7.8 ppm (fw) and 10.8 ppm (fw) showed behavioral deviations including decreased ambulatory activity and stress tolerance, and decreased swimming ability, respectively. New data on neurochemical markers in Little Brown Bats indicates that 10 ppm in the fur is a preliminary subclinical threshold, above which researchers have shown changes to bat neurochemistry (Nam et al. 2012). With the exception of Hoary Bat and Seminole Bat, every bat species we sampled had individuals with fur Hg levels that exceeded the level of concern (10 ppm) and 15% (n = 124) of our total sample exceeded that level.

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Figure 33. Study area of bat sampling locations.

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140 Maximum Level Detected

Fur Hg (ppm, ww)

120

Mean + SD

100 80 60 40 20 0

Bats Species

Figure 34. Mean plus standard deviation and maximum level detected of fur Hg concentrations in bat species sampled in New England and Mid-Atlantic States, 2006 to 2008. Red line indicates a preliminary subclinical threshold for mercury exposure in bats (10 ppm in fur of Little Brown Bats), above which researchers have shown changes to their neurochemistry (Nam et al. 2012). 6.3.2 REGIONAL MERCURY EXPOSURE Bats sampled at Little River in Southeastern NH had the highest mean fur Hg concentrations ( = 33.96 ± 37.12 ppm), due to extremely high levels in Big Brown Bats ( = 53.48 ± 42.04 ppm) (Figure 35 & 36). Pollution levels in the Little River are known to be high in this area and the US Attorney’s Office has filed complaints on behalf of the U.S. Environmental Protection Agency (EPA) against at least two industrial plants in the area for violations of the Clean Water Act (U.S. EPA 2010).

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Fur Hg Level (ppm, ww)

140

Maximum Level Detected

120

Mean + SD

100 80 60 40 20 0

Bat Sampling Areas

Figure 35. Regional mean fur Hg concentrations in bats sampled in New England and MidAtlantic States, 2006 to 2008. Fur Hg Level (ppm, ww)

140 120 100

Maximum Level Detected Mean + SD

80 60 40 20 0

Bat Species Sampled in Southeastern NH

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Figure 36. Mean and maximum level detected of fur Hg (ppm) in bats sampled near Little River, Rockingham County in Southeastern NH, 2008. Big Brown Bat fur Hg concentrations were also elevated in other regions where sampled, particularly Coastal VA and Central/Western NY ( = 15.97 ± 15.62 ppm and = 22.47 ± 13.56, respectively) (Figure 37). Eastern Small-footed Myotis had the next highest mean fur Hg level ( = 12.88 ± 4.98 ppm); however, the sample size is small (N = 7) and spread out over 3 sampling regions (Figure 38). Indiana Bats (N = 12) sampled in Southern NY and Central/Western NY had the next greatest mean fur Hg level ( = 10.58 ± 5.07 ppm) (Figure 39). Indiana Bats are a federal and NYS-listed endangered species. They were first identified as being in danger of extinction as far back as 1966 and were one of the first mammals listed as endangered under the Endangered Species Act of 1973. Indiana Bats have also been identified as a species vulnerable to population declines due to white-nose syndrome (NYSDEC 2010). Evening Bats (N = 39) sampled at Great Dismal Swamp in coastal VA had elevated mean fur Hg concentrations ( = 10.56 ± 7.93 ppm, max = 40.90 ppm). Southeastern Myotis (N = 9), also sampled at Great Dismal Swamp, had similar fur Hg levels ( = 10.50 ± 9.33 ppm, max = 25.00 ppm). Silver-haired Bats (N = 7) sampled in WV had a mean fur Hg level of 9.33 ± 3.91 ppm with a maximum level detected of 14.23 ppm. Rafinesque’s Big-eared Bats (N = 4) sampled in Great Dismal Swamp in Coastal VA had a mean fur Hg level of 8.10 ± 3.38 ppm and a maximum level detected of 12.00 ppm. Northern Long-eared Bats (Myotis septentrionalis) (N = 148) had an overall mean fur Hg concentration of 8.04 ± 6.58 ppm and maximum level detected of 41.53 ppm. Those sampled in Central/Western NY had the highest mean fur Hg concentrations ( = 16.89 ± 10.27 ppm, N = 19), which were significantly greater than levels detected in Coastal ME, WV, and Southern NY (Figure 40). Eastern Pipistrelles (N = 22) were sampled in Great Dismal Swamp in Coastal VA and WV (Figure 41). Red Bats (N = 38) were primarily sampled at Great Dismal Swamp in Coastal VA and Monongahela National Forest in WV (Figure 43); Coastal VA levels were higher ( = 5.55 ± 7.12 ppm) than WV ( = 4.46 ± 2.56 ppm) but the difference was not significant (Figure 42). Red Bats were also sampled in Coastal ME and MA, Southern NY, and the Adirondack Mts, NY but sample sizes were small. Little Brown Bats (N = 441) had the highest mean fur Hg levels in southeastern NH ( = 11.70 ± 6.08 ppm, N = 5) followed by the Adirondack Mts, NY ( = 7.55 ± 6.61 ppm, N = 60), and Coastal MA ( = 6.22 ± 4.23 ppm, N = 14) (Figure 43). Seminole Bats (N = 9) were sampled in Great Dismal Swamp and had low fur Hg levels ( = 2.68 ± 0.76 ppm). One Hoary Bat was sampled in Adirondack Park (1.63 ppm) and 5 were sampled in WV ( = 1.99 ± 0.93).

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Fur Hg Level (ppm, ww)

140 Maximum Level Detected Mean + SD

120 100 80 60

40 20 0

Big Brown Bat Sampling Regions

Figure 37. Regional mean fur Hg concentrations in Big Brown Bats sampled in New England and Mid-Atantic States, 2006 to 2008. Big brown bats sampled in NH had significantly higher fur Hg concentrations than Coastal VA, Southern NY, and WV (P < 0.05); Adirondack Mts, NY was not included in analysis due to small sample size. Fur Hg Level (ppm, ww)

50 Maximum Value Detected 40

Mean + SD

30 20 10 0

Eastern Small-footed Myotis Sampling Regions

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Figure 38. Regional mean fur Hg concentrations in Eastern Small-footed Myotis sampled in coastal ME, southern NY, and WV, 2006 to 2008. Small sample size precluded statistical analysis. 50 Fur Hg Level (ppm, ww)

Maximum Level Detected 40

Mean + SD

30 20 10 0 Central/Western NY (N = 1)

Southern NY (N = 11)

Indiana Bat Sampling Regions

Fur Hg Level (ppm, ww)

Figure 39. Regional mean and maximum levels detected of fur Hg concentrations in Indiana Bats sampled in New York State, 2006 to 2008. 50 40

Maximum Level Detected Mean + SD

30 20 10 0

Northern Long-eared Bat Sampling Regions

Figure 40. Regional means and maximum levels detected of fur Hg in Northern Long-eared Bats sampled in New England and Mid-Atlantic States, 2006 to 2008. Northern Long-eared Bats in Central/Western NY had significantly higher fur Hg levels than those sampled in

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Coastal ME, WV, and Southern NY (P < 0.0001) (Southeast NH was excluded from analysis due to small sample size).

Fur Hg Level (ppm, ww)

50 40

Maximum Level Detected Mean + SD

30 20 10 0 WV (N = 13)

Coastal VA (N = 9)

Eastern Pipistrelle Sampling Regions

Fur Hg Level (ppm, ww)

Figure 41. Regional means and maximum levels detected of fur Hg concentrations in Eastern Pipistrelles sampled in WV and Coastal VA, 2007 and 2008. 50 40

Maximum Level Detected Mean + SD

30 20 10 0

Red Bat Sampling Regions

Figure 42. Regional means and maximum levels detected of fur Hg concentrations in Red Bat sampled in New England and Mid-Atlantic States, 2006 to 2008. No significant difference was detected in fur Hg levels between Coastal VA and WV; small sample size precluded analysis of other regions.

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Fur Hg Level (ppm. ww)

50 40

Maximum Level Detected Mean + SD

30 20 10 0

Little Brown Bat Sampling Area

Figure 43. Regional means and maximum levels detected of fur Hg concentrations in Little Brown Bats sampled in New England and Mid-Atlantic States, 2006 to 2008. Little Brown Bats sampled in the Adirondack Mts, NY had significantly higher fur Hg levels than those sampled in PA, WV, and Northwest VA (P < 0.05); Southeast NH had the highest mean but was precluded from statistical analysis due to small sample size. 6.3.4 MERCURY EXPOSURE BY AGE AND SEX Adult male bats (N = 213) had a mean fur Hg level of 9.82 ± 9.66 ppm, which was significantly higher than the mean for juvenile males ( = 4.39 ± 3.42 ppm) and adult and juvenile females ( = 6.71 ± 9.29 ppm and = 2.88 ± 2.46 ppm) (P < 0.0001) (Figure 44). Adult female levels were significantly higher than both juvenile females and males (P < 0.02), while juvenile male levels were significantly higher than juvenile females (P < 0.0001). These results are similar to age and gender sensitivities detected in bats sampled at Mammoth Cave National Park, KY (Webb et al. 2006); however, the maximum fur Hg level detected in KY (10 ppm) was much less than in our samples. Bats are long-lived species (10 to 30 years) and thus have the potential to accumulate high levels of Hg over the course of a lifetime. However, it is impossible to distinguish and classify ages beyond simply juvenile (less than 12 months) and adult. Therefore, it is possible for fur Hg means for the adult age class to be skewed to the right due to a few very old individuals. Females had lower Hg levels than males despite that they have higher energy demands during the breeding season (i.e., milk production) and consequently consume more insect matter during this period, thereby increasing their exposure to mercury. This difference is likely a result of females transferring a portion of their Hg body Biodiversity Research Institute

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Fur Hg (ppm), fw

burden to their young in the uterus and through breast milk, thus reducing their own Hg levels in the process. 20 18 16 14 12 10 8 6 4 2 0 Female Juvenile (N = 122)

Male Juvenile (N = 72)

Female Adult (N = 389)

Male Adult (N = 213)

Bat Sex and Age Class

Figure 44. Mean fur Hg concentrations among male and female adult and juvenile bats sampled in New England and the Mid-Atlantic States, 2006 to 2008. Adult male bats had significantly higher (P < 0.0001) fur Hg levels than female adults and juveniles of both sexes. Female adults were significantly higher than juveniles of both sexes (P < 0.02). Male juveniles were higher than juvenile females (P < 0.0001). 6.4 CONCLUSIONS Bat fur samples are indicators of Hg body burdens, reflecting both dietary uptake and body accumulation (Mierle et al. 2000, Yates et al. 2005). Since adults live for decades, they accumulate an overall body burden of Hg, whereas juveniles less than one year old have only accumulated Hg levels from their mother’s milk and from the site where they have foraged. Bats are at risk of Hg exposure from consumption of both aquatic and terrestrial insects. However, bats may be exposed to levels of mercury high enough to cause sublethal effects if they consume large quantities of insects that spend larval stages in contaminated sediments (Hickey et al. 2001). Our results demonstrate that bats are at great risk when feeding in riparian habitats. Insectivorous bats use both aerial and gleaning techniques when foraging over river surfaces and floodplain edges. Big Brown Bats with exceptionally high Hg levels in NH were captured over a forested stream and were presumably feeding on aquatic insects. Aquatic nymphs of flying insects with elevated Hg levels were the presumed source of Hg in several aerial insectivores, including the Eastern Pipistrelle, along a point source-polluted Virginia river (Powell 1983). In terrestrial ecosystems, bats consume a variety of insect prey. Carter et al. (2003) found Northern Long-eared Bats main prey was Coleoptera and Biodiversity Research Institute

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Lepidoptera followed by Diptera, all of which have been shown in our study to accumulate mercury. In Indiana and Illinois, small beetles were the major component of the diet of Big Brown Bats (Whitaker 1995). Other studies found Northern Long-eared Bats and Little Brown Bats typically preyed on moths and beetles, but overall had a varied diet including spiders (Whitaker and Hamilton 1998, Brack and Whitaker 2001). Spiders have been shown in our study and previous studies to have elevated Hg concentrations (Adair et al. 2003, Cocking et al. 1991). Hg levels in Coleopterans (beetles) are generally low, although its feeding behavior affects the degree of concentration. For example, insectivorous invertebrates have been shown to accumulate MeHg at levels 8.5 times higher than herbivorous invertebrate species (Mason et al. 2000). However, the degree of Hg contamination and where it is concentrated in the ecosystem will also affect which species exhibit elevated MeHg levels. Larval Scarabaeidae beetles along a contaminated river floodplain in Virginia had significantly higher MeHg concentrations than larval Elateridae beetles (Cocking et al. 1991). Scarabaeidae feed on detritus, fungi, roots, tubers, and underground plant parts while Elateridae consume roots and underground stems, seedlings, and other low-trophic level insects (Peterson 1951). Underground plant parts contained greater concentrations than above ground plants and there was an abundance of Hg in soil-dwelling invertebrates at Cocking et al.’s (1991) study site indicating that the detritus food web is a significant pathway for Hg bioaccumulation. The effects of Hg in the aquatic and terrestrial food webs are detrimental to local bat populations. Most bat species in our study exceeded levels shown to have adverse effects in rodents across multiple regions, indicating that bats are at risk to Hg exposure in a variety of prey items throughout the Northeast US. These trends are not unique to the northeastern US. Hickey et al. (2001) examined fur Hg concentrations in various Chiroptera species from eastern Ontario and adjacent Quebec, Canada. In 1997, they pooled samples from five sites and found fur Hg concentrations ranging from 2.0 to 7.6 ppm, (fw). In 1998, they sampled the same sites and found fur Hg concentrations that approached or exceeded 10.0 ppm (fw). Massa and Grippo (2000) examined various Chiroptera species from rivers in Arkansas that were under fish consumption advisories and found fur Hg concentrations ranging from 1.0 to 30 ppm, (fw). They concluded that Hg accumulation had exceeded the hazard criteria set by the U.S. Fish & Wildlife Service and that Hg accumulation in bats is a serious problem that warrants further investigation. Fifteen percent of our sample exceeded the concentrations of concern for rodents (10.8 ppm) and 5 percent (N = 35) of our sample exceeded the level established for the much larger mammals, mink and otter (20 ppm) (Yates et al. 2004, 2005). These levels were observed in 6 different bat species from 6 different sampling regions indicating that freeranging bats throughout the New England and Mid-Atlantic States are at high risk of Hg exposure. Biodiversity Research Institute

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7.0 POLICY AND MANAGEMENT RECOMMENDATIONS This investigation provides critical information to policy makers regarding the pervasiveness of environmental mercury pollution in the northeastern United States. The results from this study indicate that mercury levels in songbirds, bats, and invertebrates throughout the Northeast are high enough to cause detrimental effects to populations inhabiting areas prone to bioaccumulation of mercury in the terrestrial food web. Reducing anthropogenic sources of mercury is one essential strategy for minimizing the impact of mercury on people and wildlife, but to effectively inform policy decisions at each stage of the process, scientists also need more data. We recommend a concurrent three-pronged approach for minimizing adverse impacts of mercury on wildlife: 1. Identify the species, habitats, and regions at risk to mercury exposure 2. Address synergistic interactions of mercury with other environmental pollutants 3. Minimize wildlife exposure by reducing mercury emissions. 1. Identify the species, habitats, and regions at risk to mercury exposure. The first step in identifying mercury risk is to improve mercury monitoring in both aquatic and terrestrial ecosystems across the United States, by establishing a national mercury monitoring network. Legislation for a National Mercury Monitoring Network (MercNet) was introduced into the 112th Congress (to the Senate Public Works and the House Energy and Commerce Committees) and will provide a comprehensive and standard way for measuring mercury in the air, water, soil, as well as in fish and wildlife (Schmeltz et al. 2011). Songbirds and bats are nominated as part of the mercury monitoring effort (Mason et al. 2008). Congress needs to pass legislation authorizing the creation of MercNet, which will allow the federal government to scientifically evaluate the efficacy of policy and management decisions that, in turn, will allow for better decisions in the future and protect past mercury abatement investments 2. Address synergistic interactions of mercury with other environmental pollutants There is preliminary evidence that mercury can act synergistically with other environmental stressors, such as acid deposition, making it important to develop sciencebased policy recommendations for setting air pollution thresholds to protect and restore U.S. ecosystems and species (Fenn et al. 2011). A “critical loads” approach to understanding air pollution impacts requires the assessment of multiple contaminant “loading” to sensitive ecosystems above which significant adverse impacts are detected. This strategy is accepted as superior by the scientific and regulatory communities, and is in use in Europe, Canada, and parts of the United States, but has yet to be used to understand the interaction of mercury with other contaminants. Although critical loads allow for more refined policy decisions, their establishment requires firm commitment and funding in order to enable Biodiversity Research Institute

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the most up-to-date scientific determinations. Congress should direct the U.S. EPA to implement critical loads for sulfur and nitrogen, along with thresholds for mercury, and the U.S. EPA should use these thresholds to assess progress under the Clean Air Act. 3. Minimize wildlife exposure by reducing mercury emissions. Mercury emission reduction must occur to effectively minimize wildlife exposure to mercury, but there are multiple routes that can help us achieve this goal. First, the U.S. can substantially reduce mercury emissions by implementing best available pollution control technology for coal-fired power plants. Technological pollution control for reducing mercury pollution has been enormously successful in the regulation of municipal and medical waste incinerators (Cain et al. 2011) and the U.S. EPA Mercury and Air Toxics Standards Rule will provide similar reductions for power plants with a goal of 90% less mercury emissions (U.S. EPA 2011). It is critical that we ensure implementation of this common sense solution to the largest stationary source of airborne mercury—coal-fired power plants. Second, by avoiding mercury “cap and trade” systems, we will prevent biological mercury hotspots. While “cap and trade” programs are effective in certain pollution strategies, like those for acid rain components, it is inappropriate for a pollutant like mercury. There is a growing body of evidence that local mercury emission sources, such as from coal-fired power plants, can have significant local effects on downwind ecosystems leading to the development of biological mercury hotspots (Evers et al. 2007, Driscoll et al. 2007). By avoiding mercury “cap and trade” systems, our expectation is to prevent new mercury hotspots from being created across the United States and globally. Third, the U.S. can take part in regulating global mercury emissions by supporting the UNEP Mercury Treaty. The United Nations Environment Programme (UNEP) intends to ratify a globally binding agreement on mercury in 2013 (UNEP Chemicals Branch 2011). Reductions in the purposeful use of mercury for small-scale gold mining, chlor-alkali plants, and in manufactured products are planned, while emissions from fossil-fuel burning and other sources are being negotiated. The U.S. State Department and the U.S. EPA should continue their international leadership roles in guiding new standards for global mercury pollution as well as in helping set comprehensive and standard monitoring programs. Adding new delegates from other federal agencies, such as the Department of Interior, will help facilitate greater connections with environmental mercury studies and management in the United States.

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8.0 ACKNOWLEDGEMENTS We are grateful for a grant from The Nature Conservancy’s Rodney Johnson and Katherine Ordway Stewardship Endowment that supported the development of this publication as well as parts of the original research. Data collection was made possible by funding from The Nature Conservancy, New York State Energy Research and Development Authority, New York State Department of Environmental Conservation, the Wildlife Conservation Society and the U.S. Fish and Wildlife Service. This research was the result of years of collaborations and we would like to acknowledge those that offered their assistance. Many researchers generously shared their data with us. We are deeply indebted to Dr. David Braun of Sound-Science. We thank Chris Rimmer and Kent McFarland of the Vermont Center for Eco-studies for their assistance with sampling Bicknell’s thrushes; Greg Shriver for providing samples from wood thrushes in Delaware; Sam Edmonds, Nelson O’Driscoll, and the numerous researchers involved with the International Rusty Blackbird Working Group for sharing their extensive sampling of rusty blackbirds; Jeff Loukmas from the New York State Department of Environmental Conservation for providing invertebrate mercury data; Gary Lovett from the Institute for Ecosystem Studies for supplying soil data; and Chad Seewagen from the Wildlife Conservation Society for providing multiple years of samples. Others provided field accommodations, logistical support, and helpful expertise. We thank the SUNY College of Environmental Science and Forestry’s Adirondack Ecological Center for providing access to study sites and lodging for field crews; the staff at the Montezuma National Wildlife Refuge and the Tonawanda Wildlife Management Area for site access and permits to sample birds and bats; the staff of the Marine Nature Study Area in Hempstead, NY for logistical support and assistance in the field; Al Hicks of the New York State Department of Environmental Conservation and John Chenger of Bat Conservation and Management for their assistance with providing bat samples; Cara Lee at The Nature Conservancy for helping us with field housing, logistics, and site access; Bruce Connery at Acadia National Park for helping us with field housing, permits, and site access; Dr. Ford and staff for assisting us with site selection and permission in the Fernow Experimental Forest; Bill DeLuca for assisting with sampling efforts, field housing, permits, and site access in New Hampshire; the Boy Scouts of America for providing access and a field camp at Massawepie for multiple years; the YMCA for providing housing/field camps and site access for multiple years; Bill Schuster at Black Rock Forest for providing site access and permission for multiple years; Bob Mulvihill at Powdermill Avian Research Center for providing permission, site selection, site access, sampling assistance, samples, and an incredible learning environment for multiple years; Mike Fowles and site managers at the U.S. Army Corp of Engineers for providing site permits/access and enthusiastically Biodiversity Research Institute

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assisting with Pennsylvania field logistics; Tom LeBlanc of Allegany State Park for providing site selection recommendations, logistical support, field housing, and overall enthusiasm for our project; the staff at numerous National Wildlife Refuges including Rachel Carson NWR (ME), Wertheim NWR (NY), Parker River NWR (MA), Ninigret NWR (RI), McKinney NWR (CT); Maine Department of Inland Fisheries and Wildlife; Jen Walsh at the University of New Hampshire for field assistance; and Henry Caldwell of Dome Island for providing all kinds of help with boats, field housing, and permits, as well as being a gracious host for multiple years. We are especially grateful to the staff of Cornell’s Lab of Ornithology, Conservation Science department, for their support of this project. In particular, we thank James D. Lowe for all his devoted work in the field, banding birds and collecting soil, leaves, and bird samples, and for his assistance with preparing the metadata; Maria Stager for her aid in bird sampling and banding; Kenneth V. Rosenberg for his departmental support; and Kevin Webb, from Cornell’s Lab of Ornithology, Information Science department, for his excellent GIS support. Within The Nature Conservancy, we appreciate those who supported this work over the years including: David Higby, Peter Kareiva, Mark King, Cara Lee, Nicole Maher, Rebecca Shirer, Brad Stratton, Troy Weldy, and Alan White.

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Rimmer, C. C., K. P. McFarland, D. C. Evers, E. K. Miller, Y. Aubry, D. Busby, and R.J. Taylor. 2005. Mercury levels in Bicknell’s Thrush and other insectivorous passerine birds in montane forests of the northeastern United States and Canada. Ecotoxicology 14:223-240. Rimmer, C. C., E. K. Miller, K. P. McFarland, R. J. Taylor, and S. D. Faccio. 2010. Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19: 697 – 709. Robertson, R. J., B. J. Stutchbury, and R. R. Cohen. 1992. Tree Swallow (Tachycineta bicolor). The Birds of North America Online (A. Poole, Ed.). Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/011. Robinson, W.D. 1995. Louisiana waterthrush (Seiurus motacilla). The Birds of North America Online (A. Poole, Ed.). Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/151. Rosenberg, K. V. 2008. Louisiana Waterthrush species account in The Second Atlas of Breeding Birds in New York State (McGowan and Corwin, eds). Published by Cornell University Press, Ithaca, NY, USA. TheRumbold, D. G., S. L. Niemczyk, L. E. Fink, T. Chandraesekhar, B. Harkanson and K. A. Lane. 2001. Mercury in eggs and feathers of Great Egrets (Ardea albus) from Florida Everglades. Archives of Environmental Contaminants and Toxicology 41: 501-507. Sauer, J. R., J. E. Hines, and J. Fallon. 2008. The North American Breeding Bird Survey, Results and Analysis 1966 - 2007. Version 5.15.2008. USGS Patuxent Wildlife Research Center, Laurel, MD. Scheuhammer, A. M. 1987. The chronic toxicity of aluminum, cadmium, mercury, and lead in birds: a review. Environmental Pollution. 46:263-95. Scheuhammer, A. M. 1991. Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environmental Pollution 71:329-375. Scheuhammer, A. M. 1996. Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environmental Pollution 94:337343. Biodiversity Research Institute

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Schmeltz, D., D. C. Evers, C. T. Driscoll, R. Artz, M. Cohen, D. Gay, R. Haeuber, D. P. Krabbenhoft, R. Mason, K. Morris, and J.G. Weiner. 2011. MercNet: a national monitoring network to assess responses to changing mercury emissions in the United States. Ecotoxicology 20:1713-1725. Schroeder, W. H. and J. Munthe. 1998. Atmospheric mercury – An overview. Atmospheric Environment 32: 809–822. Schwesig, D. and E. Matzner. 2000. Pools and fluxes of mercury and methylmercury in two forested catchments in Germany. Science of the Total Environment 260: 213–223. Seigneur C., K. Lohman, K. Vijayaraghavan, and R. Shia. 2003. Contributions of global and regional sources to mercury deposition in New York State. Environmental Pollution 123: 365-373. Senn, D. B., E. J. Chsney, J. D. Blum, M. S. Bank, A. Maage, and J. P. Shine. 2010. Stable isotope (N,C, Hg) study of methylmercury sources and trophic transfer in the northern Gulf of Mexico. Environmental Science and Technology 44: 1630-1637. Shriver, G., D. C. Evers, T. Hodgman, R. Taylor. 2006. Saltmarsh Sharp-tailed Sparrows as indicators of methlymercury availability in estuaries. Environmental Bioindicators 2: 129 – 135. Silver, T. M. and T. D. Nudds. 1995. Influence of low level cadmium and reduced calcium intake on tissue Cd concentrations and behavior of American Black Ducks. Environmental Pollution 90:153-161. St. Louis, V. L., J. W. M Rudd, C. A. Kelly, B. D Hall, K. R. Rolfus, K. J. Scott, S. E. Lindberg and W. Dong. 2001. Importance of the forest canopy to fluxes of methyl mercury and total mercury to boreal ecosystems. Environmental Science and Technology 35: 3089–3098. Tremblay, A., M. Lucotte, M. Meili, L. Cloutier, and P. Pichet. 1996. Total mercury and methylmercury contents of insects from boreal lakes: ecological, spatial, and temporal patterns. Water Quality Research Journal of Canada 31:851 – 873. UNEP Chemicals Branch. 2011. http://www.unep.org/hazardoussubstances/Mercury/tabid/ 434/Default.aspx.

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U.S. Environmental Protection Agency (U.S. EPA). 2010. New Releases By Date. . Accessed 13 December 2010. U.S. EPA. 2011. Mercury and Air Toxics Standards. http://www.epa.gov/mats. VanArsdale, A., J. Weiss, G. Keeler, E. Miller, G. Boulet, R. Brulotte, L. Poissant. 2005. Patterns of mercury deposition and concentration in northeastern North America (1996-2002). Ecotoxicology 14:37-52. Verschuuren, H. G., R. Kroes, E. M., Den Tonkelaar, J. M.,Berkvens, P. W. Helleman, A. G. Rauws, P. L. Schuller, and G. J. Van Esch. 1976. Toxicity of methylmercury chloride in rats. III. Long-term toxicity study. Toxicology 6:107-23. Wada, H., D. A. Cristol, F. M. A. McNabb and W. A. Hopkins. 2009. Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environmental Science and Technology 43(15):6031 – 6038. Walker, L. A., V. R. Simpson, L. Rockett, C. L. Wienburg, and R. F. Shore. 2007. Heavy metal contamination in bats in Britain. Environmental Pollution 148: 483 – 490. Walters, D. M., M. C. Mills, K. M. Fritz, and D. F. Raikow. 2010. Spider-mediated flux of PCBs from contaminated sediments to terrestrial ecosystems and potential risks to arachnivorous birds. Environmental Science and Technology 44: 2949-2956. Webb, C. J., L. M. Clark, B. Carson, K. Helf, M. Ruck, and S. Dawadi. 2006. A survey of mercury bioaccumulation in bats at Mammoth Cave National Park. Presented at the Philadelphia Annual Meeting, 22 – 25 October 2006. Whitaker. J. O. 1995. Food of the Big Brown Bat (Eptesicus fuscus) from maternity colonies in Indiana and Illinois. American Midland Naturalist 134:346–360. Whitaker, J. O and W. J. Hamilton. 1998. Mammals of the Eastern United States, Comstock Pub. Associates, Ithaca, NY. Wiener, J., P. Krabbenhoft, G. Heinz, and A. Scheuhammer. 2003. Ecotoxicology of Mercury, in Handbook of Ecotoxicology, pp 409 - 463, 2nd edition, Hoffman, D., Rattner, B., Burton, A., and Cairns, J., Eds. Lewis Publishers, Boca Raton, FL. Biodiversity Research Institute

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10.0 Appendix A. Common and Latin Names of Songbirds Sampled for Blood Hg Concentrations. Common Name Acadian Flycatcher American Goldfinch American Redstart American Robin Barn Swallow Bicknell's Thrush Black-and-White Warbler Black-capped Chickadee Black-thoated Blue Warbler Black-throated Green Warbler Blue-headed Vireo Bobolink Brown Creeper Brown Thrasher Carolina Chickadee Carolina Wren Cedar Waxwing Cerulean Warbler Chipping Sparrow Cliff Swallow Common Grackle Common Yellowthroat Dark-eyed Junco Eastern Kingbird Eastern Phoebe Eastern Towhee Eastern Wood-Pewee Grasshopper Sparrow Gray Catbird Great Crested Flycatcher Hermit Thrush Hooded Warbler House Wren Biodiversity Research Institute

Latin Name Empidonax virescens Spinus tristus Setophaga ruticilla Turdis migratorius Hirundo rustica Catharus bicknelli Mniotilta varia Poecile atricapilla Dendroica caerulescens Dendroica virens Vireo solitarius Dolichonyx oryzivorus Certhia americana Toxostoma rufum Poecile carolinensis Thryothorus ludovicianus Bombycilla cedrorum Dendroica cerulea Spizella passerina Petrochelidon pyrrhonota Quiscalus quiscula Geothlypis trichas Junco hyemalis Tyrannus tyrannus Sayornis phoebe Pipilo erythrophthalmus Contopus virens Ammodramus savannarum Dumetella carolinensis Myiarchus crinitus Catharus guttatus Wilsonia citrina Troglodytes aedon Page 89

Indigo Bunting Least Flycatcher Lincoln's Sparrow Louisiana Waterthrush Magnolia Warbler Marsh Wren Mourning Warbler Myrtle Warbler (Yellow-rumped) Nelson's Sparrow Northern Cardinal Northern Parula Northern Rough-winged Swallow Northern Waterthrush Ovenbird Prairie Warbler Red-breasted Nuthatch Red-eyed Vireo Red-winged Blackbird Rose-breasted Grosbeak Rusty Blackbird Saltmarsh Sparrow Savannah Sparrow Scarlet Tanager Seaside Sparrow Song Sparrow Swainson's Thrush Swamp Sparrow Traill's Flycatcher (Willow/Alder) Tree Swallow Tufted Titmouse Veery White-breasted Nuthatch White-eyed Vireo White-throated Sparrow Winter Wren Wood Thrush Worm-eating Warbler Yellow Palm Warbler Yellow-bellied Flycatcher Yellow-throated Vireo Biodiversity Research Institute

Passerina cyanea Empidonax minimus Melospiza lincolnii Parkesia moacilla Dendroica magnolia Cistothorus palustris Oporornis philadelphia Dendroica coronata Ammodramus nelsoni Cardinalis cardinalis Parula americana Stelgidopteryx serripennis Parkesia noveboracensis Seiurus aurocapillus Dendroica discolor Sitta canadensis Vireo olivaceus Agelaius phoeniceus Pheucticus ludovicanus Euphagus carolinus Ammodramus caudacutus Passerculus sandwichensis Piranga olivacea Ammodramus maritimus Melospiza melodia Catharus ustulatus Melospiza georgiana Empidonax traillii/E. alnorum Tachycineta bicolor Baeolophus bicolor Catharus fuscescens Sitta carolinensis Vireo griseus Zonotrichia albicollis Troglodytes troglodytes Hylocichla mustelina Helmitheros vermivorus Setophaga palmarum Empidonax flaviventris Vireo flavifrons Page 90

Yellow-throated Warbler

Biodiversity Research Institute

Setophaga dominica

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11.0 Appendix B – SONGBIRD MERCURY EXPOSURE BY SPECIES N

Mean Blood Hg Level (ppm) ± SD

Range

States Sampled

5

0.0468 ± 0.0231

0.0122 – 0.0691

VA

Indigo Bunting

11

0.2538 ± 0.4810

0.0169 – 1.6700

NY, VA

Northern Cardinal

2

0.1824 ± 0.1564

0.0718 – 0.2930

VA

Rose-breasted Grosbeak

1

0.0241



NY

Scarlet Tanager

10

0.0645 ± 0.0387

0.0179 - 0.1180

NY, PA, VA

1

0.0897



NY

Chipping Sparrow

3

0.2200 ± 0.1330

0.1260 - 0.3140

ME, PA

Eastern Towhee

1

0.0761



NY

Grasshopper Sparrow

1

0.0502



VA

Lincoln's Sparrow

23

0.1574 ± 0.1697

0.0128 - 0.6640

ME, NY

Nelson's Sparrow

97

0.5412 ± 0.3440

0.1070 - 2.0000

MA, ME

Saltmarsh Sparrow

479

0.7531 ± 0.4779

0.0292 - 3.7300

CT, MA, ME, NY, RI

Savannah Sparrow

2

0.0221 ± 0.0023

0.0205 – 0.0237

NY

Slate-colored Junco

4

0.0484 ± 0.0378

0.0200 – 0.1030

ME, NY, VA

Species

Bombycillidae Cedar Waxwing

Cardinalidae

Certhiidae Brown Creeper

Emberizidae

Song Sparrow

109

0.1423 ± 0.1162

0.0157 - 0.5226

MA, ME, NY, PA, RI, VA

Swamp Sparrow

4

0.2043 ± 0.0348

0.1568 – 0.2384

MA, NY

Seaside Sparrow

8

0.4924 ± 0.2333

0.1470 - 0.7749

CT, NY

White-throated Sparrow

3

0.0124 ± 0.0006

0.0131 – 0.0120

ME

3

0.0039 ± 0.0029

0.0058 - 0.0005

ME, VA

Barn Swallow

5

0.1304 ± 0.0281

0.1053 - 0.1660

ME

Cliff Swallow

25

0.2067 ± 0.0925

0.0840 - 0.4710

ME

Northern Rough-winged Swallow

2

0.0414 ± 0.0068

0.0366 - 0.0462

VA

Fringillidae American Goldfinch

Hirundinidae

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Range

States Sampled

5

Mean Blood Hg Level (ppm) ± SD 0.1997 ± 0.0176

0.1830 - 0.2180

ME

Bobolink

2

0.0327 ± 0.0253

0.0148 - 0.0506

CT, ME

Common Grackle

3

0.1294 ± 0.0339

0.0963 - 0.1640

VA

Red-winged Blackbird

40

0.2380 ± 0.2355

0.0115 - 9.418

MA, ME, NY, VA

Rusty Blackbird

93

0.6555 ± 0.4111

0.0931 - 1.066

ME, NH, VT

Brown Thrasher

1

0.0567



PA

Gray Catbird

2

0.0589 ± 0.0018

0.0576 - 0.0602

PA

Black-capped Chickadee

11

0.1007 ± 0.0739

0.0113 - 0.2300

NY, PA

Boreal Chickadee

1

0.0683



ME

Carolina Chickadee

1

0.0308



VA

Tufted Titmouse

3

0.0944 ± 0.0761

0.0448 - 0.1820

NY, VA

American Redstart

15

0.0633 ± 0.0405

0.0173 - 0.1860

NY, PA

Black and White Warbler

3

0.0623 ± 0.0131

0.0474 - 0.0717

NY, PA

Blackpoll Warbler

21

0.0575 ± 0.0140

0.0343 - 0.0817

ME, NH, NY

Black-throated Blue Warbler

8

0.0472 ± 0.0210

0.0175 - 0.0704

NY, VA

Black-throated Green Warbler

5

0.0541 ± 0.0308

0.0243 - 0.1060

NH, NY, VA

Blue-winged Warbler

1

0.0719



VA

Cerulean Warbler

3

0.0163 ± 0.0047

0.0118 - 0.0211

PA

Common Yellowthroat

15

0.1585 ± 0.1139

0.0365 - 0.4057

CT, MA, ME, NY, PA

Hooded Warbler

7

0.0815 ± 0.0567

0.0306 - 0.1780

NY, PA, VA

Louisiana Waterthrush

20

0.2073 ± 0.1489

0.0527 - 0.6202

NY, PA, VA

Magnolia Warbler

10

0.1209 ± 0.0834

0.0419 - 0.2900

ME, NH, NY, PA

Mourning Warbler

1

0.0169



NY

Myrtle Warbler

8

0.1217 ± 0.0845

0.0671 - 0.3180

ME, NY

Northern Parula

1

0.0351



VA

Species

N

Tree Swallow Icteridae

Mimidae

Paridae

Parulidae

Biodiversity Research Institute

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Range

States Sampled

6

Mean Blood Hg Level (ppm) ± SD 0.2346 ± 0.1706

0.0746 - 0.5660

ME, NY

Ovenbird

37

0.0514 ± 0.0500

0.0102 - 0.2950

ME, NY, PA, VA

Prairie Warbler

1

0.0420



NY

Worm-eating Warbler

5

0.0712 ± 0.0612

0.0236 - 0.1610

NY, VA

Yellow Palm Warbler

9

0.5643 ± 0.4082

0.1940 - 1.4900

NY

Yellow-throated Warbler

2

0.2640 ± 0.2022

0.121 – 0.407

VA

Red-breasted Nuthatch

1

0.1440



NY

White-breasted Nuthatch

4

0.1131 ± 0.0814

0.0664 – 0.2350

NY, PA, VA

Carolina Wren

28

0.1865 ± 0.1206

0.0172 - 0.5160

VA

House Wren

1

0.123



PA

Marsh Wren

2

0.2450 ± 0.0028

0.2430 - 0.2470

CT

Winter Wren

1

0.0646



NH

American Robin

16

0.0716 ± 0.0589

0.0039 - 0.1910

ME, NY, PA, VA, VT, WV

Bicknell's Thrush

50

0.1231 ± 0.1224

0.0130 - 0.7946

ME, NH, NY, VT

Hermit Thrush

113

0.0683 ± 0.0552

0.0143 - 0.5130

ME, NH, NY, PA, VT

Swainson's Thrush

56

0.0832 ± 0.0383

0.0296 - 0.2380

ME, NH, NY, VT

Veery

104

0.0517 ± 0.0323

0.0034 - 0.1648

MA, NH, NY, PA, VA, VT, WV

Wood Thrush

160

0.0881 ± 0.0759

0.0016 - 0.6923

DE, ME, NY, PA, VA, WV

Acadian flycatcher

12

0.2934 ± 0.1314

0.1320 - 0.5230

VA

Eastern Kingbird

1

0.0807



NY

Eastern Phoebe

3

0.1653 ± 0.0726

0.0886 - 0.2330

NY, VA

Eastern Wood-Pewee

2

0.8688 ± 0.4293

0.5653 - 1.1723

NY

Great Crested Flycatcher

2

0.1629 ± 0.0398

0.1347 - 0.1910

NY, VA

Least Flycatcher

1

0.15812



NY

Traill's Flycatcher

6

0.2966 ± 0.2254

0.1160 - 0.7130

MA, NY

Species

N

Northern Waterthrush

Sittidae

Troglodytidae

Turdidae

Tyrannidae

Biodiversity Research Institute

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Range

States Sampled

3

Mean Blood Hg Level (ppm) ± SD 0.1208 ± 0.0613

0.0780 - 0.1910

NH, NY

6

0.0859 ± 0.0736

0.0149 - 0.2050

NY, PA, VT

153

0.0957 ± 0.0819

0.0080 - 0.5140

MA, ME, NY, PA, VA, VT, WV

White-eyed Vireo

2

0.0360 ± 0.0141

0.0260 - 0.0460

PA

Yellow-throated Vireo

2

0.3944 ± 0.4544

0.0731 - 0.7157

NY, VA

Species

N

Yellow-bellied Flycatcher Vireonidae Blue-headed Vireo Red-eyed Vireo

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Blood Hg (ppm), ww

12.0 Appendix C – SONGBIRD MERCURY EXPOSURE BY FAMILY 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0

Maximum Species Value Detected Mean + SD

Cardinalidae

Figure 45. Mean plus standard deviation of blood Hg concentrations in Cardinalidae species. 4.0 Blood Hg (ppm), ww

3.5

Maximum Species Level Detected Mean + SD

3.0 2.5 2.0 1.5 1.0 0.5 0.0

Emberizidae

Figure 46. Mean and maximum level detected of blood Hg concentrations in Emberizidae species. Biodiversity Research Institute

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Blood Hg (ppm), ww

1.0 Maximum Species Level Detected 0.8

Mean + SD

0.6 0.4 0.2 0.0

Hirundinidae

Figure 47. Mean and maximum blood Hg concentrations in Hirundinidae species.

Blood Hg (ppm), ww

2.4 2.0

Maximum Species Level Detected Mean + SD

1.6 1.2 0.8 0.4 0.0

Icteridae

Figure 48. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Icteridae species.

Biodiversity Research Institute

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1.0 Blood Hg (ppm), ww

Maximum Level Detected 0.8

Mean + SD

0.6 0.4 0.2 0.0 Carolina Chickadee (N = 1)

Boreal Chickadee (N = 1)

Eastern Tufted Titmouse (N = 3)

Black-capped Chickadee (N = 13)

Paridae

Figure 49. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Paridae species. 1.6

Blood Hg (ppm), ww

1.4 1.2

Maximum Species Level Detected Mean + SD

1.0 0.8 0.6 0.4 0.2 0.0

Parulidae

Figure 50. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Parulidae species.

Biodiversity Research Institute

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1 Blood Hg Level (ppm), ww

Maximum Level Detected 0.8

Mean + SD

0.6 0.4 0.2 0 Red-breasted Nuthatch (N = 1)

White-breasted Nuthatch (N = 4)

Sittidae

Figure 51. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Sittidae species.

Blood Hg (ppm), ww

1.0 Maximum Species Level Detected 0.8

Mean + SD

0.6 0.4 0.2 0.0

Troglodytidae

Figure 52. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Troglodytidae species.

Biodiversity Research Institute

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Blood Hg (ppm), ww

1.0 0.8

Maximum Species Level Detected Mean + SD

0.6 0.4 0.2 0.0

Vireonidae

Figure 53. Mean plus standard deviation and maximum level detected of blood Hg concentrations in Vireonidae species.

Biodiversity Research Institute

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