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Article
Production and Retention of Methylmercury in Inundated Boreal Forest Soils Kristofer R Rolfhus, James P. Hurley, Richard A Bodaly, and Gregory Perrine Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es505398z • Publication Date (Web): 10 Feb 2015 Downloaded from http://pubs.acs.org on February 18, 2015
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 29
Environmental Science & Technology
1
Production and Retention of Methylmercury in Inundated Boreal Forest Soils
2
Kristofer R. Rolfhus1*, James P. Hurley2, Richard A. (Drew) Bodaly3, and Gregory
3
Perrine1
4 5
Author Addresses:
6
* corresponding author; email: [email protected]; phone: 608-785-8289; fax: 608-
7
785-8281
8
1
Wisconsin-La Crosse, La Crosse, WI 54601
9 10
2
13
Department of Civil and Environmental Engineering, Environmental Chemistry and Technology Program, University of Wisconsin-Madison, Madison, WI 53706
11 12
Department of Chemistry and Biochemistry, River Studies Center, University of
3
Penobscot River Mercury Study, 115 Oystercatcher Place, Salt Spring Island, BC, Canada V8K 2W5
14 15 16 17 18 19 20 21 22 23 24
1
ACS Paragon Plus Environment
Environmental Science & Technology
25 26
TOC/Abstract Art:
27 28
Abstract
29
The Flooded Uplands Dynamics Experiment (FLUDEX) was an ecosystem-scale study
30
examining the production of methylmercury (MeHg) and greenhouse gases from
31
reservoirs constructed on an upland boreal forest landscape in order to quantify their
32
dependence upon carbon stores. We detail the within-reservoir production and storage of
33
MeHg before, during, and nine years after the experiment. The reservoirs were net
34
MeHg producers during the first two years of flooding, and net demethylating systems
35
afterwards. During years 1-3, a rapid pulse of MeHg and total Hg was observed in
36
floodwater, followed by substantial increases in MeHg in seston and sediment. Re-
37
sampling of the dry reservoirs nine years after the experiment ended indicated that
38
organic soil MeHg was still 8 to 52-fold higher than pre-flood conditions, and averaged
39
86% of the levels recorded at the end of the third flooding year. Both total Hg and MeHg
40
retention in soil were a strong function of organic carbon content. The timescale of soil
41
MeHg retention may help explain the decadal time lag frequently observed for the
42
decrease of piscivorous fish Hg concentrations in new reservoirs. Predicted extreme
2
ACS Paragon Plus Environment
Page 2 of 29
Page 3 of 29
Environmental Science & Technology
43
precipitation events associated with climate change may serve to make landscapes more
44
susceptible to this process.
45 46
Keywords: mercury, methylmercury, soil, flooding, inundation, reservoir
47 48 49
Introduction Mercury (Hg) contamination of aquatic and terrestrial systems has led to elevated
50
concentrations in ecosystems and food webs and enhanced exposure of the neurotoxin
51
methylmercury (MeHg) to humans and wildlife1,2. Mercury is methylated by aquatic
52
bacteria at oxic/anoxic interfaces, which may be exacerbated in reservoir systems that
53
experience water level change. For example, changes in the Hg content of age-0 yellow
54
perch (Perca flavescens) in lakes within Voyageurs National Park, MN, were linked to
55
changes in water level from the previous year3, while a survey of 18 Finnish boreal
56
reservoirs linked fish Hg levels to reservoir age and water level fluctuation4. While
57
MeHg may be formed rapidly on timescales of weeks to months, its effects may be
58
lasting; elevated predatory fish Hg values have been observed for 10-30 years in
59
Canadian reservoirs5.
60
Methylation is enhanced by elevated levels of inorganic mercury, sulfate ion, and
61
organic matter, with a growing evidence of association with the metabolism of a variety
62
of aquatic microbes, including iron reducing, methanogenic, acetogenic, and cellulolytic
63
species 6-10. Mercury exhibits a high degree of association with soil organic matter,
64
forming complexes that are strongly dependent upon thiol content11,12. Indeed, sulfur
65
redox cycling may play an important role in MeHg formation in periodically flooded
3
ACS Paragon Plus Environment
Environmental Science & Technology
66
ecosystems13 where sulfate is reduced microbially and oxidized by drying events and
67
sulfide oxidizing bacteria as observed in a Canadian reservoir14 and the Florida
68
Everglades15. The rate of supply of organic matter to inundated ecosystems is also an
69
important factor, whether the source is from the flooded soil, vegetation, marginal
70
erosion, or is autochthonous in origin16.
71
Soils and surficial vegetation are important sinks for mercury deposition, with an
72
estimated global anthropogenic enrichment factor of 5.8 for the rapidly-exchangeable
73
terrestrial Hg pool17. Recent work suggests that there may be an increasing latitudinal
74
trend in soil Hg and MeHg storage, possibly due to slower carbon cycling, vegetation
75
type, or condensation/evaporation cycles18,19.
76
Inundation represents a potentially large vector for Hg re-mobilization into food
77
webs. For periodically inundated systems, production of MeHg may be greatest in soils
78
that contain the highest levels of inorganic Hg, labile organic matter, and moderate levels
79
of porewater sulfate during flooding14,20,21. It is unclear whether MeHg production is a
80
function of the preceding duration of dry conditions. One possibility is that due to
81
continuous atmospheric Hg and sulfate deposition, longer dry periods would result in
82
increased MeHg associated with the labile organic matter pool. Predictions from the
83
latest Intergovernmental Panel on Climate Change Technical Summary22 and the 3rd
84
National Climate Assessment23 state that storm effects and coastal surges are likely to
85
become stronger through the 21st century, with precipitation becoming flashier and more
86
extreme. Resultant seasonal flooding and high-precipitation events may therefore
87
enhance MeHg formation and exposure to food webs in terrestrial ecosystems. The
4
ACS Paragon Plus Environment
Page 4 of 29
Page 5 of 29
Environmental Science & Technology
88
potential exists for similar effects in flooded coastal zones, but these remain largely
89
unconstrained.24,25
90
The first ecosystem-level study to investigate inundation effects on MeHg
91
formation examined an experimentally-flooded boreal forest wetland at the Experimental
92
Lakes Area (ELA; northwestern Ontario, Canada), and termed the “ELA Reservoir
93
Project (ELARP)”26,27. This study, thought to represent a “worst-case scenario” of
94
flooding a wetland ecosystem, found that MeHg was rapidly produced from peat, though
95
most of what was produced was not hydrologically or atmospherically exported27. A
96
similar recent study was conducted in the Florida Everglades21, where a constructed
97
wetland was a net source for MeHg during the first two years of flooding, and a sink
98
afterwards.
99
The follow-up study to ELARP, the Flooded Uplands Dynamics Experiment
100
(“FLUDEX”), measured MeHg production and greenhouse gas emission relative to a
101
gradient of stored C in three experimentally inundated upland boreal forest
102
catchments28,29. Prior FLUDEX papers have focused on construction of a reservoir mass
103
balance29 and effects of reservoir creation on Hg in zooplankton30. Here, we present
104
additional results from the FLUDEX project that test the hypothesis that flood-derived
105
soil MeHg is retained over annual time scales. Herein, we detail 1) the response of
106
MeHg and total mercury in boreal forest soils to cyclic inundation, 2) evidence of flooded
107
soils as the principal source of MeHg to the reservoirs, and 3) the relationship between
108
Hg and C in reservoir components before, during, and after the project.
109 110
Experimental
5
ACS Paragon Plus Environment
Environmental Science & Technology
111
Study Location.
112
Three sub-hectare reservoirs were created at the Experimental Lakes Area,
113
Ontario, Canada (Figure SI-1; Table SI-1). The high-C reservoir contained substantially
114
more total carbon (soil plus vegetation) than the medium and low reservoirs, and
115
possessed far more soil carbon relative to the medium and low reservoirs, which were of
116
similar quantity. The high-C reservoir was a mixed wet-dry forest composed of paper
117
birch (Betula papyrifera), jack pine (Pinus banksiana), black spruce (Picea maricana),
118
Labrador tea (Ledum groenlandicum), and mosses (Sphagnum spp. and Polytrichum
119
spp.)29. The medium-C reservoir was a dry forest ecosystem of mainly birch, jack pine,
120
and shrubs (Vaccinium spp. and Alnus spp.), while the ridge-top low-C reservoir was
121
approximately 70% dry birch/jack pine forest and 30% exposed granitic bedrock covered
122
by lichen. The soils were characterized as poor, acidic brunisols of Precambrian granitic
123
origin31, whose depth ranged from bare bedrock in the low-C reservoir to approximately
124
1 m in the high-C reservoir. The reservoirs were filled and drained annually from 1999
125
(“Year 1”) through 2003 (“Year 5”). Feed water from a nearby oligotrophic lake (Roddy
126
Lake) was continuously pumped into the reservoirs during the summer period, and
127
flowed out of a notched weir at the opposite end of the inlet. Typical hydraulic residence
128
times were on the order of one week (Table SI-1), and water depth was on average
129
approximately 1 meter. Reservoirs were typically filled in late May/early June, and
130
drained in late September/early October. The average duration of inundation was
131
approximately 100 days.
132 133
Sample Collection
6
ACS Paragon Plus Environment
Page 6 of 29
Page 7 of 29
134
Environmental Science & Technology
The initial “pre-flood” Hg content of each site was determined by collecting intact
135
soil cores every 20 m along two crossing transects (total 29 cores; September 1998), as
136
well as 9 cores for detailed vertical profiling that were 0.050). However, samples from the high-C reservoir
10
ACS Paragon Plus Environment
Page 10 of 29
Page 11 of 29
Environmental Science & Technology
225
associated with patches of peat were up to 20-fold higher in MeHg than soils just 10 m
226
away. For mineral soils, total Hg was significantly higher in the high-C relative to the
227
low-C reservoir, and MeHg was significantly higher in the high-C compared to the
228
medium-C reservoir (p
Article
Production and Retention of Methylmercury in Inundated Boreal Forest Soils Kristofer R Rolfhus, James P. Hurley, Richard A Bodaly, and Gregory Perrine Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es505398z • Publication Date (Web): 10 Feb 2015 Downloaded from http://pubs.acs.org on February 18, 2015
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 29
Environmental Science & Technology
1
Production and Retention of Methylmercury in Inundated Boreal Forest Soils
2
Kristofer R. Rolfhus1*, James P. Hurley2, Richard A. (Drew) Bodaly3, and Gregory
3
Perrine1
4 5
Author Addresses:
6
* corresponding author; email: [email protected]; phone: 608-785-8289; fax: 608-
7
785-8281
8
1
Wisconsin-La Crosse, La Crosse, WI 54601
9 10
2
13
Department of Civil and Environmental Engineering, Environmental Chemistry and Technology Program, University of Wisconsin-Madison, Madison, WI 53706
11 12
Department of Chemistry and Biochemistry, River Studies Center, University of
3
Penobscot River Mercury Study, 115 Oystercatcher Place, Salt Spring Island, BC, Canada V8K 2W5
14 15 16 17 18 19 20 21 22 23 24
1
ACS Paragon Plus Environment
Environmental Science & Technology
25 26
TOC/Abstract Art:
27 28
Abstract
29
The Flooded Uplands Dynamics Experiment (FLUDEX) was an ecosystem-scale study
30
examining the production of methylmercury (MeHg) and greenhouse gases from
31
reservoirs constructed on an upland boreal forest landscape in order to quantify their
32
dependence upon carbon stores. We detail the within-reservoir production and storage of
33
MeHg before, during, and nine years after the experiment. The reservoirs were net
34
MeHg producers during the first two years of flooding, and net demethylating systems
35
afterwards. During years 1-3, a rapid pulse of MeHg and total Hg was observed in
36
floodwater, followed by substantial increases in MeHg in seston and sediment. Re-
37
sampling of the dry reservoirs nine years after the experiment ended indicated that
38
organic soil MeHg was still 8 to 52-fold higher than pre-flood conditions, and averaged
39
86% of the levels recorded at the end of the third flooding year. Both total Hg and MeHg
40
retention in soil were a strong function of organic carbon content. The timescale of soil
41
MeHg retention may help explain the decadal time lag frequently observed for the
42
decrease of piscivorous fish Hg concentrations in new reservoirs. Predicted extreme
2
ACS Paragon Plus Environment
Page 2 of 29
Page 3 of 29
Environmental Science & Technology
43
precipitation events associated with climate change may serve to make landscapes more
44
susceptible to this process.
45 46
Keywords: mercury, methylmercury, soil, flooding, inundation, reservoir
47 48 49
Introduction Mercury (Hg) contamination of aquatic and terrestrial systems has led to elevated
50
concentrations in ecosystems and food webs and enhanced exposure of the neurotoxin
51
methylmercury (MeHg) to humans and wildlife1,2. Mercury is methylated by aquatic
52
bacteria at oxic/anoxic interfaces, which may be exacerbated in reservoir systems that
53
experience water level change. For example, changes in the Hg content of age-0 yellow
54
perch (Perca flavescens) in lakes within Voyageurs National Park, MN, were linked to
55
changes in water level from the previous year3, while a survey of 18 Finnish boreal
56
reservoirs linked fish Hg levels to reservoir age and water level fluctuation4. While
57
MeHg may be formed rapidly on timescales of weeks to months, its effects may be
58
lasting; elevated predatory fish Hg values have been observed for 10-30 years in
59
Canadian reservoirs5.
60
Methylation is enhanced by elevated levels of inorganic mercury, sulfate ion, and
61
organic matter, with a growing evidence of association with the metabolism of a variety
62
of aquatic microbes, including iron reducing, methanogenic, acetogenic, and cellulolytic
63
species 6-10. Mercury exhibits a high degree of association with soil organic matter,
64
forming complexes that are strongly dependent upon thiol content11,12. Indeed, sulfur
65
redox cycling may play an important role in MeHg formation in periodically flooded
3
ACS Paragon Plus Environment
Environmental Science & Technology
66
ecosystems13 where sulfate is reduced microbially and oxidized by drying events and
67
sulfide oxidizing bacteria as observed in a Canadian reservoir14 and the Florida
68
Everglades15. The rate of supply of organic matter to inundated ecosystems is also an
69
important factor, whether the source is from the flooded soil, vegetation, marginal
70
erosion, or is autochthonous in origin16.
71
Soils and surficial vegetation are important sinks for mercury deposition, with an
72
estimated global anthropogenic enrichment factor of 5.8 for the rapidly-exchangeable
73
terrestrial Hg pool17. Recent work suggests that there may be an increasing latitudinal
74
trend in soil Hg and MeHg storage, possibly due to slower carbon cycling, vegetation
75
type, or condensation/evaporation cycles18,19.
76
Inundation represents a potentially large vector for Hg re-mobilization into food
77
webs. For periodically inundated systems, production of MeHg may be greatest in soils
78
that contain the highest levels of inorganic Hg, labile organic matter, and moderate levels
79
of porewater sulfate during flooding14,20,21. It is unclear whether MeHg production is a
80
function of the preceding duration of dry conditions. One possibility is that due to
81
continuous atmospheric Hg and sulfate deposition, longer dry periods would result in
82
increased MeHg associated with the labile organic matter pool. Predictions from the
83
latest Intergovernmental Panel on Climate Change Technical Summary22 and the 3rd
84
National Climate Assessment23 state that storm effects and coastal surges are likely to
85
become stronger through the 21st century, with precipitation becoming flashier and more
86
extreme. Resultant seasonal flooding and high-precipitation events may therefore
87
enhance MeHg formation and exposure to food webs in terrestrial ecosystems. The
4
ACS Paragon Plus Environment
Page 4 of 29
Page 5 of 29
Environmental Science & Technology
88
potential exists for similar effects in flooded coastal zones, but these remain largely
89
unconstrained.24,25
90
The first ecosystem-level study to investigate inundation effects on MeHg
91
formation examined an experimentally-flooded boreal forest wetland at the Experimental
92
Lakes Area (ELA; northwestern Ontario, Canada), and termed the “ELA Reservoir
93
Project (ELARP)”26,27. This study, thought to represent a “worst-case scenario” of
94
flooding a wetland ecosystem, found that MeHg was rapidly produced from peat, though
95
most of what was produced was not hydrologically or atmospherically exported27. A
96
similar recent study was conducted in the Florida Everglades21, where a constructed
97
wetland was a net source for MeHg during the first two years of flooding, and a sink
98
afterwards.
99
The follow-up study to ELARP, the Flooded Uplands Dynamics Experiment
100
(“FLUDEX”), measured MeHg production and greenhouse gas emission relative to a
101
gradient of stored C in three experimentally inundated upland boreal forest
102
catchments28,29. Prior FLUDEX papers have focused on construction of a reservoir mass
103
balance29 and effects of reservoir creation on Hg in zooplankton30. Here, we present
104
additional results from the FLUDEX project that test the hypothesis that flood-derived
105
soil MeHg is retained over annual time scales. Herein, we detail 1) the response of
106
MeHg and total mercury in boreal forest soils to cyclic inundation, 2) evidence of flooded
107
soils as the principal source of MeHg to the reservoirs, and 3) the relationship between
108
Hg and C in reservoir components before, during, and after the project.
109 110
Experimental
5
ACS Paragon Plus Environment
Environmental Science & Technology
111
Study Location.
112
Three sub-hectare reservoirs were created at the Experimental Lakes Area,
113
Ontario, Canada (Figure SI-1; Table SI-1). The high-C reservoir contained substantially
114
more total carbon (soil plus vegetation) than the medium and low reservoirs, and
115
possessed far more soil carbon relative to the medium and low reservoirs, which were of
116
similar quantity. The high-C reservoir was a mixed wet-dry forest composed of paper
117
birch (Betula papyrifera), jack pine (Pinus banksiana), black spruce (Picea maricana),
118
Labrador tea (Ledum groenlandicum), and mosses (Sphagnum spp. and Polytrichum
119
spp.)29. The medium-C reservoir was a dry forest ecosystem of mainly birch, jack pine,
120
and shrubs (Vaccinium spp. and Alnus spp.), while the ridge-top low-C reservoir was
121
approximately 70% dry birch/jack pine forest and 30% exposed granitic bedrock covered
122
by lichen. The soils were characterized as poor, acidic brunisols of Precambrian granitic
123
origin31, whose depth ranged from bare bedrock in the low-C reservoir to approximately
124
1 m in the high-C reservoir. The reservoirs were filled and drained annually from 1999
125
(“Year 1”) through 2003 (“Year 5”). Feed water from a nearby oligotrophic lake (Roddy
126
Lake) was continuously pumped into the reservoirs during the summer period, and
127
flowed out of a notched weir at the opposite end of the inlet. Typical hydraulic residence
128
times were on the order of one week (Table SI-1), and water depth was on average
129
approximately 1 meter. Reservoirs were typically filled in late May/early June, and
130
drained in late September/early October. The average duration of inundation was
131
approximately 100 days.
132 133
Sample Collection
6
ACS Paragon Plus Environment
Page 6 of 29
Page 7 of 29
134
Environmental Science & Technology
The initial “pre-flood” Hg content of each site was determined by collecting intact
135
soil cores every 20 m along two crossing transects (total 29 cores; September 1998), as
136
well as 9 cores for detailed vertical profiling that were 0.050). However, samples from the high-C reservoir
10
ACS Paragon Plus Environment
Page 10 of 29
Page 11 of 29
Environmental Science & Technology
225
associated with patches of peat were up to 20-fold higher in MeHg than soils just 10 m
226
away. For mineral soils, total Hg was significantly higher in the high-C relative to the
227
low-C reservoir, and MeHg was significantly higher in the high-C compared to the
228
medium-C reservoir (p
