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
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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.
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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
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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
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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
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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.
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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
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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
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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
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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
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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
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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).
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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).
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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
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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).
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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.
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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.
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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
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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).
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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
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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.
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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
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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
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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
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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
Biodiversity Research Institute
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.
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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.
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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.
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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.
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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.
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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
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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.
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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
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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
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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
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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.
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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.
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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
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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
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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
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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.
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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
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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
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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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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
Page 91
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
Biodiversity Research Institute
Page 92
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
Page 93
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
Page 94
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
Biodiversity Research Institute
Page 95
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
Page 96
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
Page 97
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
Page 98
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
Page 99
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
Page 100