United States
Environmental Protection
^^Bml M lkAgency
EP A/600/R-20/278
September 2020
www.epa. gov/ncea/isa
Integrated Science Assessment
for Oxides of Nitrogen, Oxides of
Sulfur, and Particulate Matter—
Ecological Criteria
(Final)
Center for Public Health and Environmental Assessment
Office of Research and Development
U.S. Environmental Protection Agency
Research Triangle Park, NC
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Disclaimer
This document has been reviewed in accordance with the U.S. Environmental Protection
Agency policy and approved for publication. Mention of trade names or commercial
products does not constitute endorsement or recommendation for use.
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EXECUTIVE SUMMARY
ES.1 Purpose and Scope of the Integrated Science Assessment
This Integrated Science Assessment (ISA) for Oxides of Nitrogen, Oxides of Sulfur, and
Particulate Matter—Ecological Criteria is a comprehensive evaluation and synthesis of
the most policy-relevant science aimed at characterizing the ecological effects caused by
these criteria pollutants.1 These criteria pollutants are reviewed here together because
they all contribute to nitrogen (N) and sulfur (S) deposition, which causes substantial
ecological effects. In this document, the term "oxides of nitrogen" refers to total oxidized
N (NOy), including nitric oxide (NO) and nitrogen dioxide (NO2) and all other gaseous
and particulate oxidized N containing compounds formed from NO and NO2.2 Total
sulfur oxides (SOx) includes gaseous chemical species (e.g., sulfur dioxide [SO2], sulfur
monoxide [SO], disulfur monoxide [S2O], and sulfur trioxide [SO3]) as well as particulate
species, such as ammonium sulfate [(NH^SO^ (U.S. EPA. 2011). Particulate species
include SOx species like sulfites (SO32 ) and sulfates (S042 ). but among these two
species usually only SO42 make a major contribution to particulate mass. Throughout
this document SOx is defined as the sum of SO2 and particulate sulfate (S042 ), which
together represent virtually all of the SOx mass in the atmosphere.3 Particulate matter
(PM) is composed of some or all of the following components: nitrate (NO3 ). SO42 .
ammonium (NH4 ), metals, minerals (dust), and organic and elemental carbon.
This ISA serves as the scientific foundation for the review of the ecological effects
associated with the secondary (welfare-based) National Ambient Air Quality Standards
(NAAQS) for NOy, SOx, and PM. The health effects of these criteria pollutants are
considered in separate assessments for NOy (U.S. EPA. 2016b). SOx (U.S. EPA. 2016a).
and PM (U.S. EPA. 2019V4 The Clean Air Act definition of welfare effects includes, but
is not limited to, effects on soils, water, wildlife, vegetation, visibility, weather, and
1 The general process for developing an ISA, including the framework for evaluating weight of evidence and
drawing scientific conclusions and causal judgments, is described in a companion document, Preamble to the
Integrated Science Assessments (U.S. EPA. 2015). www.epa.gov/isa.
2 This ISA reserves the abbreviation NOx strictly as the sum of NO and NO2—consistent with its use in the
atmospheric science community—and uses the term "oxides of nitrogen" to refer to the broader list of oxidized
nitrogen species. Oxides of nitrogen refers to NOy as the total oxidized nitrogen in both gaseous and particulate
forms. The major gaseous and particulate constituents of NOy include nitric oxide (NO), nitrogen dioxide (NO2),
nitric acid (HNO3), peroxyacetyl nitrate (PAN), nitrous acid (HONO), organic nitrates, and particulate nitrate
(NO3 ). This ISA uses the definitions adopted by the atmospheric sciences community.
3 The same definition of SOx used in the 2011 NOxSOx Policy Assessment (U.S. EPA. 2011).
4 In this ISA, the blue electronic links can be used to navigate to cited materials as well as appendices, sections,
tables, figures, and studies from this ISA.
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climate, as well as effects on man-made materials, economic values, and personal
comfort and well-being.
The current secondary NAAQS for NOy and SOx were set to protect against direct
damage to vegetation by NO2 or SO2. The secondary NAAQS for NO2 is identical to the
primary standard set in 1971: an annual average not to exceed 0.053 ppm N dioxide. The
secondary NAAQS for SO2, set in 1973, is a 3-hour average of 0.5 ppm SO2, not to be
exceeded more than once per year. The current secondary standards for PM are intended
to address PM-related visibility and nonvisibility welfare effects. These standards are a
3-year annual mean PM2 5 concentration of 15 |ig/nr\ with the 24-hour average PM2 5 and
PM10 set at concentrations of 35 |ig/m3 and 150 |ig/nr\ respectively.
This ISA updates the 2008 ISA for Oxides of Nitrogen and Oxides of Sulfur—Ecological
Criteria [hereafter referred to as 2008 ISA (U.S. EPA. 2008)1. as well as the ecological
portion of the 2009 ISA for Particulate Matter (U.S. EPA. 2009) with studies and reports
published from January 2008 through May 2017. There are some studies included that
were published more recently than the May 2017 literature cutoff date; these studies were
added based on recommendations from the Clean Air Scientific Advisory Committee
(CASAC). The U.S. EPA conducted in-depth searches to identify peer-reviewed
literature on relevant topics. Subject-matter experts and the public were also able to
recommend studies and reports during a kick-off workshop held by the U.S. EPA in
March 2014 for NOy and SOx and in June 2016 for PM. CASAC recommended the
inclusion of additional studies during the review of the first draft. To fully describe the
state of available science, the U.S. EPA also carried over the most relevant studies from
previous assessments to include in this ISA.
This ISA determines whether NOy, SOx, and PM concentrations in the air or deposition
from the air cause ecological effects. The ecological effects of deposition are grouped
into three main categories: (1) acidification (caused by gaseous NOy, SOx, and
particulate NH4+, NO3 , S042 ). (2) N enrichment/N driven eutrophication (caused by
gaseous NOy and particulate NH44" and NO3 ). and (3) S enrichment (caused by SOx and
particulate forms of S042 ). Ecological effects are further subdivided into terrestrial,
wetland, freshwater, and estuarine/near-coastal ecosystems. These ecosystems and effects
are linked by the connectivity of terrestrial and aquatic habitats through biogeochemical
pathways ofN and S.
A schematic of the document organization is given by Figure ES-1. The Integrated
Synthesis (IS) brings together key information on specific subject matter found in the
appendices. Appendix 1 is an introduction to the purpose and organization of the material
covered in Appendix 2-Appendix 16. Appendix 2 characterizes the sources and
atmospheric processes involving NOy, SOx, and PM, as well as trends in ambient
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concentrations and deposition. Appendix 3 describes direct effects of gas-phase NOy and
SOx on plants and lichens. Appendix 4 describes N and S deposition effects on terrestrial
biogeochemistry, and Appendix 5 and Appendix 6 describe the biological effects of
terrestrial acidification and terrestrial N enrichment, respectively. Appendix 7 describes
N and S deposition effects on aquatic biogeochemistry. Appendix 8 through Appendix 10
characterize the biological effects of freshwater acidification, freshwater N enrichment,
and marine eutrophication, respectively. Appendix 11 describes the effects ofN
deposition on wetlands. Appendix 12 describes the wetland and freshwater effects of S
enrichment. Appendix 13 discusses the climate modification of ecosystem response to N
and S deposition, and Appendix 14 presents information on N and S deposition effects on
ecosystem services. Information on the ecological effects of forms of PM beyond those
related to N or S deposition is presented in Appendix 15 (the nonecological welfare
effects associated with PM, such as visibility, climate, and material effects, are
considered as part of a separate review of PM [81 FR 87933, December 6, 2016]).
Appendix 16 includes six locations in the U.S. selected as case study areas that are
candidates for additional analysis of risk and exposure. These candidate sites were
selected because they have abundant data on ecological effects.
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Integrative
Synthesis
Deposition of
N and S
(Appendix 2}
Exposure
Ambient Air Concentrations
(Appendix 2}
Direct exposure
Soil and aquatic biogeochemical pathways of
acidification (NOY+ NHX +SOx)
N enrichment/eutrophication (NOY +NHX)
S nutrient (SOx)
Terrestrial Ecosystems
Direct to organism/deposition
Directto soil, effects on soil biogeochemistry (Appendix 4)
Wetland Ecosystems
Directto soil and surface water, runoff from soil
Wetland biogeochemistry (Appendices 11&12)
Freshwater Ecosystems
Directto surface water, runoff from soil, effects on
freshwater biogeochemistry (Appendix 7)
Estuaries Ecosystems
Directto water, transport from watershed runoff, effects on
biogeochemistry along the freshwater to ocean continuum
(Appendix 7}
Climate Modification of Ecosystem
Response to N and S
(Appendix 13)
Ecosystem
Services
(Appendix 14)
Biological Effects
S02, N02, NO, PAN, HN03
(Appendix 3)
Plant foliar and lichen Injury
]
Biological effects of
acidification (NOY+ NHX +SOx)
N enrichment/eutrophication (NOy +NHX)
S nutrient (SQX)
Terrestrial Ecosystems
Acidification (Appendix 5)
N enrichment/eutrophication (Appendix 6)
Wetlands Ecosystems
N enrichment/eutrophication (Appendix 11)
S nutrient (Appendix 12)
Freshwater Ecosystems
Acidification (Appendix 8)
N enrichment/eutrophication (Appendix 9)
S nutrient (Appendix 12)
Estuarine Ecosystems
N nutrient/ eutrophication (Appendix 10)
N enhanced ocean acidification (Appendix 10)
Other Ecological
Effects of PM
(Appendix 15)
Case
Studies
(Appendix 16)
HN03 = nitric acid; N = nitrogen; NHX = reduced nitrogen; NO = nitric oxide; N02 = nitrogen dioxide; NOy = nitrogen oxides;
PAN = peroxyacetyl nitrate; PM = particulate matter; S = sulfur; S02 = sulfur dioxide; SOx = sulfur oxides.
Figure ES-1 Roadmap of the Integrated Science Assessment (ISA) linking
atmospheric concentrations and deposition, soil and aquatic
biogeochemistry, and biological effects.
ES.2 Emissions, Ambient Air Concentrations, and Deposition
The atmospheric chemistry from emission to deposition discussed in this ISA1 is for the
criteria pollutants NOy, SOx, and PM. NOy and SOx cause ecological effects in the gas
phase and/or after N and S deposition to surfaces. Particulate matter (PM) effects
discussed in this document focus on N and S containing species, which together usually
make up a large fraction of the P\l;> mass in most areas of the U.S. HHj§
(NHX = NH3 + NH4+) includes both gas-phase NH3 and the PM component NH4 . NH3 is
estimated to account for 19-63% of total observed inorganic N deposition, depending on
region (Appendix 2.1). Therefore, NH? is discussed in this ISA along with NOy and
relevant PM components to better understand and compare their contributions to both wet
and dry N deposition.
1 The term concentration is used throughout the ISA to denote either a mass per unit volume or a volume per unit
volume (mixing ratio). The use of concentration to denote abundance expressed as mixing ratio is firmly entrenched
in the literature; therefore, it is retained here.
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Both gaseous and particulate forms of NOy, SOx, and NHX contribute to atmospheric wet
and dry deposition. The major components of PM in the U.S. are NO3 , SO42 . NH/,
organic matter, elemental C, crustal material, and sea salt. Of these, NO3 . S042 , and
NH4+ usually have a strong influence on acid deposition, and NO3 and NH4+, and in
some cases organic N (organic nitrates and reduced organic N), contribute substantially
to N deposition and eutrophication.
The sources and precursors to gaseous and particulate forms of NOy, SOx, and NHx vary.
The main contributors to acidifying precipitation are formed from precursor emissions of
the gases SO2, NOx, and NH3 (Appendix 2.2). Electricity-generating units (EGUs) are the
source of about half of national gaseous emissions of SO2, mainly from coal-fired power
plants. Notably, SO2 emissions from EGUs have been decreasing. NOx emissions have a
wider distribution of sources, with substantial contributions from highway and
off-highway vehicles, lightning, and EGUs. Fertilizer application and animal waste are
the main national-scale sources of NH3, with animal waste contributing the most. Primary
PM2 5 and PM10 emissions are dominated by dust and combustion products of fires, but
much of the PM2 5 mass in the U.S. is produced by reaction of gas-phase precursors to
form secondary PM2 5. In this process, particulate NH4+, NO3 . and SO42 are primarily
derived from the gaseous precursors NH3, NOx, and SO2 (Appendix 2.3). Formation of
particulate N and S is described in the 2019 ISA for Particulate Matter (U.S. EPA. 2019).
An understanding of the sources, chemistry, and atmospheric processes for these
gas-phase and PM species is necessary to understand acidifying and N deposition.
Since the passage of the Clean Air Act Amendments in 1990, the emissions of NOx and
SO2 have declined dramatically. Total emissions of SO2 decreased by 89% from 1990 to
2017, resulting in a decrease in SO2 concentrations of 89% in the eastern U.S. and 45% in
the western U.S. Emissions of NOx in the U.S. declined by 61% between 1990 and 2017,
while nationwide annual average 98th percentile NO2 concentrations decreased by 53%
from 1990 to 2017. These reductions have in turn led to decreases in PM2 5 concentrations
because of declines in the amount of S042 and NO3 produced, and a decrease in the
fraction of PM2 5 accounted for by SO42 . Between 1989 and 2017, average particulate
S042 concentration decreased by 75% in the eastern U.S. and 35% in the western U.S.,
and average particulate NO3 concentration decreased by 51% in the eastern U.S. and
37% in the western U.S.
Averaged across the contiguous U.S., deposition of total N (oxidized + reduced N, in kg
N/ha/yr) has changed only slightly since 2000 (Appendix 2.6.2). Figure ES-2 shows that
between 2000 and 2018 large decreases in oxidized nitrogen (Figure ES-2A) have
combined with large increases in reduced nitrogen deposition (Figure ES-2B) to produce
a small decrease in total nitrogen deposition (Figure ES-2C). There is large spatial
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variability in N deposition over the contiguous U.S. (Figure ES-2C). According to
National Atmospheric Deposition Program Total Deposition Committee's (TDEP s)
estimates for 2016-2018 (Appendix 2.6.2), much of the eastern U.S. is estimated to
receive at least 10 kg N/ha/yr dry + wet deposition, with some areas receiving more than
15 kg N/ha/yr. Figure ES-2 A through C shows that between 2000 and 2018, large
decreases in oxidized nitrogen deposition occurred.
2000-2002
2016-2018
A)
Oxidized
Nitrogen •
* .
'< 4 —
\ |
B)
Reduced
Nitrogen
Mi
m
f*
C)
Total
Nitrogen
D)
Total
Sulfur
r/*"
li
tl
w
Ha = hectare; kg = kilogram; N = nitrogen; OxN = oxidized nitrogen; ReN = reduced nitrogen; S = sulfur.
Source: We acknowledge the Total Deposition (TDep) Science Committee of the National Atmospheric Deposition Program (NADP)
for their role in making the TDep data and maps available.
Figure ES-2 Wet plus dry deposition of (A) oxidized nitrogen, (B) reduced
nitrogen, (C) total nitrogen, and (D) total sulfur over the 3-year
periods 2000-2002 and 2016-2018.
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For S, wet deposition tends to dominate over dry deposition in large areas of the
contiguous U.S. However, in some regions, mostly in the west, dry deposition of mainly
SO2 is greater than wet deposition. Anthropogenic emissions of S and subsequent
deposition have declined markedly since the 1990s, with the most pronounced declines in
the eastern U.S., as shown in Figure ES-2D. Currently, the highest values of total
(wet + dry) SOx deposition in the U.S. are in parts of the Ohio Valley region where they
range between 15 and 20 kg S/ha/yr.
Both N and S deposition contribute to acidification of ecosystems. The acidity of
rainwater has decreased, as indicated by the increase of rainwater pH across the U.S.
since 1990, coincident with decreases in the wet deposition of nitrate and sulfate.
However, widespread areas are still affected by acidifying precipitation, mainly in the
eastern U.S. (see Appendix 2.6.1). Total acidifying deposition (wet + dry N + S,
expressed as H+ equivalents) fluxes for 2016 to 2018 ranged from a few tenths of H+
keq/ha/yr over much of the western U.S. to over 1.5 H+ keq/ha/yr in parts of the Midwest
and the Mid-Atlantic regions, and in other isolated hotspots surrounding areas of
concentrated industrial or agricultural activity (Figure IS-6). Estimated deposition fluxes
greater than 1.5 keq/ha/yr covered amuch smaller portion of the U.S. in 2016-2018 than
in 2000-2002.
ES.3 Ecological Effects
In this ISA, information on ecological effects from controlled exposure, field addition,
ambient deposition, and toxicological studies, among others, are integrated to form
conclusions about the causal nature of relationships between NOy, SOx, and PM and
ecological effects. Studies on the ecological effects are considered in relation to a range
of ambient concentration and deposition loads that are within two orders of magnitude
from current conditions [Preamble (U.S. EPA. 2015). Section 5c]. A consistent and
transparent framework [Preamble (U.S. EPA. 2015). Table II] is applied to classify the
ecological effect evidence according to a five-level hierarchy:
1. Causal relationship
2. Likely to be a causal relationship
3. Suggestive of, but not sufficient to infer, a causal relationship
4. Inadequate to infer a causal relationship
5. Not likely to be a causal relationship
The conclusions presented in Table ES-1 are based on recent findings integrated with
information from the 2008 ISA (U.S. EPA. 2008). The conclusions of Table ES-1 are
based on careful consideration of errors and uncertainty in the supporting studies. We
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also consider the coherence of findings integrated across studies of underlying
geochemical and biological mechanisms. There are 18 causality statements in this ISA
(Table ES-1). Fourteen are causal relationships repeated from the 2008 ISA or modified
from the 2008 ISA to include specific endpoints. For these causality statements, new
research strengthens the evidence base and is consistent with the 2008 ISA. There is one
likely causal relationship repeated from the 2009 ISA for Particulate Matter. Three causal
relationships are new endpoint categories not evaluated in the 2008 ISA. Although NOy
and SOx can cause phytotoxic injury, current monitored concentrations of gas-phase NOy
and SOx are not high enough to injure vegetation. For all other identified causal
relationships identified in this ISA, the evidence indicates a causal association from
current levels of S and/or N deposition.
Table ES-1 Causal determinations for relationships between criteria pollutants
and ecological effects from the 2008 NOx/SOx Integrated Science
Assessment (ISA) or the 2009 ISA for Particulate Matter (PM), for
other effects of PM, and the current draft ISA.
Causal Determination
Effect Category
2008 NOX/SOX ISA
Current Draft ISA
Gas-phase direct phytotoxic effects
Gas-phase SO2 and injury to vegetation
Causal relationship
Causal relationship
Section IS.3 and Appendix 3.6.1
Gas-phase NO, NO2, and PAN and injury to vegetation
Causal relationship
Causal relationship
Section IS.3 and Appendix 3.6.2
Gas-phase HNO3 and injury to vegetation3
Causal relationship
Causal relationship
Section IS.3 and Appendix 3.6.3
N and acidifying deposition to terrestrial ecosystems
N and S deposition and alteration of soil biogeochemistry in
terrestrial ecosystems'5
Causal relationship
Causal relationship
Section IS.5.1 and Appendix 4.1
N deposition and the alteration of the physiology and growth of
terrestrial organisms and the productivity of terrestrial
ecosystems0
Not included
Causal relationship
Section IS.5.2 and Appendix 6.6.1
N deposition and the alteration of species richness, community
composition, and biodiversity in terrestrial ecosystems0
Causal relationship
Causal relationship
Section IS.5.2 and Appendix 6.6.2
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Table ES-1 (Continued): Causal determinations for relationships between criteria
pollutants and ecological effects from the 2008 NOx/SOx
Integrated Science Assessment (ISA) or the 2009 ISA for
Particulate Matter (PM), for other effects of PM, and the
current draft ISA.
Causal Determination
Effect Category
2008 NOX/SOX ISA
Current Draft ISA
Acidifying N and S deposition and the alteration of the physiology
and growth of terrestrial organisms and the productivity of
terrestrial ecosystemsd
Not included
Causal relationship
Section IS.5.3 and Appendix 5.7.1
Acidifying N and S deposition and the alteration of species
richness, community composition, and biodiversity in terrestrial
ecosystemsd
Causal relationship
Causal relationship
Section IS.5.3 and Appendix 5.7.2
N and acidifying deposition to freshwater ecosystems
N and S deposition and alteration of freshwater biogeochemistrye
Causal relationship
Causal relationship
Section IS.6.1 and Appendix 7.1.7
Acidifying N and S deposition and changes in biota, including
physiological impairment and alteration of species richness,
community composition, and biodiversity in freshwater
ecosystems'
Causal relationship
Causal relationship
Section IS.6.3 and Appendix 8.6
N deposition and changes in biota, including altered growth and
productivity, species richness, community composition, and
biodiversity due to N enrichment in freshwater ecosystems9
Causal relationship
Causal relationship
Section IS.6.2 and Appendix 9.6
N deposition to estuarine ecosystems
N deposition and alteration of biogeochemistry in estuarine and
near-coastal marine systems
Causal relationship
Causal relationship
Section IS.7.1 and Appendix 7.2.10
N deposition and changes in biota, including altered growth, total
primary production, total algal community biomass, species
richness, community composition, and biodiversity due to N
enrichment in estuarine environments11
Causal relationship
Causal relationship
Section IS.7.2 and Appendix 10.7
N deposition to wetland ecosystems
N deposition and the alteration of biogeochemical cycling in
wetlands
Causal relationship
Causal relationship
Section IS.8.1 and Appendix 11.10
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Table ES-1 (Continued): Causal determinations for relationships between criteria
pollutants and ecological effects from the 2008 NOx/SOx
Integrated Science Assessment (ISA) or the 2009 ISA for
Particulate Matter (PM), for other effects of PM, and the
current draft ISA.
Causal Determination
Effect Category
2008 NOX/SOX ISA
Current Draft ISA
N deposition and the alteration of growth and productivity, species
physiology, species richness, community composition, and
biodiversity in wetlands
Causal relationship
Causal relationship
Section IS.8.2 and Appendix 11.10
S deposition to wetland and freshwater ecosystems
S deposition and the alteration of mercury methylation in surface
water, sediment, and soils in wetland and freshwater ecosystems'
Causal relationship
Causal relationship
Section IS.9.1 and Appendix 12.7
S deposition and changes in biota due to sulfide phytotoxicity,
including alteration of growth and productivity, species physiology,
species richness, community composition, and biodiversity in
wetland and freshwater ecosystems
Not included
Causal relationship
Section IS.9.2 and Appendix 12.7
2009 PM ISA
Current Draft ISA
Other ecological effects of PM
PM and a variety of effects on individual organisms and
ecosystems
Likely to be a causal
relationship
Likely to be a
causal relationship
Section IS.10 and Appendix 15.8
C = carbon; Hg = mercury; HN03 = nitric acid; ISA = Integrated Science Assessment; N = nitrogen; NO = nitric oxide;
N02 = nitrogen dioxide; PAN = peroxyacetyl nitrate; S = sulfur; S02 = sulfur dioxide.
aThe 2008 ISA causality statements for gas-phase HN03 was phrased as "changes in vegetation."
bThe 2008 ISA included two causality statements for terrestrial biogeochemistry phrased as "relationship between acidifying
deposition and changes in biogeochemistry" and "relationship between N deposition and the alteration of biogeochemical cycling
of N."
The 2008 ISA causality statement for biological effects of N enrichment in terrestrial ecosystems was phrased as "relationship
between N deposition and the alteration of species richness, species composition, and biodiversity."
dThe 2008 ISA causality statement for biological effects of acidifying deposition in terrestrial ecosystems was phrased as
"relationship between acidifying deposition and changes in terrestrial biota."
eThe 2008 ISA included three causality statements for freshwater biogeochemistry phrased as "relationship between acidifying
deposition and changes in biogeochemistry related to aquatic ecosystems," "relationship between N deposition and the alteration
of biogeochemical cycling of N," and "relationship between N deposition and the alteration of biogeochemical cycling of C."
'The 2008 ISA causality statement for biological effects of acidifying deposition in freshwater ecosystems was phrased as
"relationship between acidifying deposition and changes in aquatic biota."
9The 2008 ISA causality statement for biological effects of N deposition in freshwater ecosystems was phrased as "relationship
between N deposition and the alteration of species richness, species composition, and biodiversity in freshwater aquatic
ecosystems."
hThe 2008 ISA causality statement for biological effects of N deposition to estuaries was phrased as "relationship between N
deposition and the alteration of species richness, species composition, and biodiversity in estuarine ecosystems."
'The 2008 ISA causality statement for biological effects of S deposition effects on ecosystems was phrased as "relationship
between S deposition and increased methylation of Hg, in aquatic environments where the value of other factors is within
adequate range for methylation."
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Figure ES-3 presents a visualization of the causality statements integrated into a single
diagram. There is not a one-to-one correspondence between the number of causality
statements, of which there are 18, and the cells indicated to have causal relationships in
the diagram because some causal statements include effects across more than one level of
biological organization. The main findings are that gaseous NOy and SOx cause
phytotoxic effects, while N and S deposition cause alteration in (1) biogeochemical
components of soil and water chemistry and (2) multiple levels of biological organization
ranging from physiological processes to shifts in biodiversity and ecological function.
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NOx SOx PM Integrated Science Assessment for Ecological Effects*
Indicator
Gases * Nitrogen Deposition Sulfur Deposition ^'oepolrtion^
Class of Pollutant Effect
Direct
Phytotoxic N-enrichment/Eutrophication Sulfide Toxicity Mercury Methylation Acidification
Ecosystem
Terrestrial Terrestrial Wetland Fresh Water Estuary Wetland Fresh Water Wetland Fresh Water Terrestrial Fresh Water
| Scale of Ecological Response
Population
Geochemistry Individual Community Ecosystem
Individual
Productivity
Biodiversity
Growth rate
Physiological
alteration, stress
or injury
Soil or sediment
chemistry
Surface water
chemistry
Causal
Not likely
Inadequate
Suggestive
Likely causal
Not evaluated in causal framework
Causality framework
*A causal relationship is likely to exist between deposition of PM and a variety of effects on individual organisms and ecosystems, based
on information from the previous review and limited new findings in this review
* Includes: NO, N02, HN03, S02, and PAN
Figure ES-3 Causal relationships between the criteria pollutants and ecological effects.
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ES.4 Direct Phytotoxic Effects of Gas-Phase Oxides of Nitrogen
(NOy) and Oxides of Sulfur (SOx)
The current NO2 and SO2 secondary NAAQS are set to protect against direct damage to
vegetation by exposure to gas-phase oxides of NOy and SOx. NH3 can also have direct
phytotoxic effects, but reduced N gases such as NH3 are not criteria air pollutants.
Research continues to support causal relationships between SO2, NO2, NO, peroxyacetyl
nitrate (PAN), HNO3, and injury to vegetation (e.g., visible foliar injury, damage to
photosynthesis, decline of growth and abundance; (Table IS-1, Section IS.4, Appendix 3),
but research that tests plant response to the lower exposure levels representative of
current atmospheric NOy and SOx concentrations is limited. Consequently, few studies
are available to help determine whether current monitored concentrations of gas-phase
NOy and SOx are high enough to injure vegetation. It is also known that these can be
gases taken up by plants and alter the N cycle in some ecosystems.
ES.5 Ecological Effects of Nitrogen and Sulfur Deposition
It is clear from the body of evidence that NOy, SOx, and PM contribute to total N and S
deposition. In turn, N and S deposition cause alteration of the biogeochemistry and the
physiology of organisms, resulting in harmful declines in biodiversity in terrestrial,
freshwater, wetland, and estuarine ecosystems in the U.S. Decreases in biodiversity mean
that some species become relatively less abundant and may be locally extirpated. In
addition to the loss of unique living species, the decline in total biodiversity can be
harmful because biodiversity is an important determinant of the stability of ecosystems
and their ability to provide socially valuable ecosystem services (see more on biodiversity
in Section IS.2.2.4).
ES.5.1 Acidification of Terrestrial and Freshwater Ecosystems
Several decades of research have documented that N and S deposition cause freshwater
and terrestrial ecosystem acidification in the U.S. New evidence strengthens the causal
relationships for ecosystem acidification determined in the 2008 ISA (Table IS-1).
Many of the terrestrial and freshwater ecosystems most sensitive to acidification in the
U.S. are found in the Northeast and Southeast. In the West, freshwater and terrestrial
ecosystems acidified from deposition are now limited in extent and occur mostly in
high-elevation sites. Watershed sensitivity to acid inputs depends on characteristics such
as underlying geology (Appendix 4 and Appendix 7) and the sensitivity of species in the
local biological community (Appendix 5 and Appendix 8). Regional heterogeneity of
deposition levels that cause ecological effects are in part due to historic exposure and
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climate. In the East, especially the southern Appalachian Mountains, and the Northeast,
the effects of acidifying deposition have been studied for several decades.
Acidified aquatic habitats have a lower number of species (species richness) of fishes,
macroinvertebrates, and phytoplankton. The effects of acidifying deposition on aquatic
ecosystems also include physiological impairment or mortality of sensitive species and
shifts in biodiversity of both flora and fauna. Organisms at all trophic levels are affected
by acidification, with clear linkages to chemical indicators for effects on algae,
zooplankton, benthic invertebrates, and fish. Acid-neutralizing capacity (ANC) is a
measure of the buffering capacity of natural waters against acidification. Even though
ANC does not directly alter the health of biota, it is a key metric of acidification that
relates to pH and aluminum levels. Biological effects are primarily attributable to low pH
and high inorganic aluminum concentration. Characterization of ANC and its levels of
concern have not changed appreciably with the newly available information since the
2008 ISA. Few or no fish species are found in lakes and streams that have very low ANC
(near zero) and low pH (near 5.0), and the number of fish species generally increases
with higher ANC and pH (Appendix 8.3). The fish lost to acidification include culturally
and recreationally important species.
Acidified terrestrial habitats are characterized by the detrimental physiological effects
seen on vegetation, including inhibited growth and decreased plant health. Acidifying
deposition can decrease membrane stability and freezing tolerance in young red spruce
needles. For many species, calcium (Ca) depletion from the soil and aluminum
mobilization cause decreased root uptake of Ca and disrupt fine root physiological
functions. Reduced availability of (base) cations in the soil can also make trees more
vulnerable to other stresses, such as damage from insects and other pathogens. Within the
eastern U.S., the physiological effects of acidifying deposition have been well
documented for the several culturally and commercially important tree species with
known ecosystem services, particularly sugar maple (Acer saccharum) and red spruce
(Picea rubens). Consistent and coherent evidence available before and since the 2008
ISA suggests acidifying deposition among these species can decrease foliar cold
tolerance, increase rates of crown dieback, decrease tree growth, suppress seedling
regeneration, and increase mortality rates. (Section IS.5.3; Appendix 5). Since the 2008
ISA, studies from the northeastern U.S. have shown that Ca addition can alleviate many
of these effects, demonstrating that acidification effects can be ameliorated in the short
term by soil amendments, suggesting the potential for recovery. However, Ca additions
have been studied in only a few areas. Acidifying deposition has also been linked to
changes in forest understory plant community composition in the northeastern U.S., grass
and forb biodiversity in eight ecoregions across the U.S., and decreased grassland plant
species richness in Europe.
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Examples of improvement in acidification have been documented in some aquatic
ecosystems in the regions most affected. Along with those improvements in acidification,
chemical recovery has been observed in the Northeast, as seen by trends in water quality
indicators (NO3 , SO42 . pH, ANC, inorganic monomeric Al, MeHg) towards inferred
preindustrial values or, in the case of inorganic Al and MeHg, below water quality
threshold values protective of biota and human health. Chemical recovery has not been
observed in studies of the southern Appalachians. In a few examples in the Northeast,
chemical recovery co-occurs with the movement of biological indicators toward
recovery. However, biological recovery has been highly variable among ecosystems and
taxonomic groups. Biological recovery lags behind, sometimes by decades, chemical
recovery. In addition, the biological recovery trajectory may exhibit hysteresis, in which
a system does not follow the same path from acidification to recovery. Most biological
communities studied to date where signs of reversal are found have not returned to
preacidification conditions and are unlikely to do so, given the extirpation of some
species, fundamental alterations in function and structure, decade-long depletion of base
cations, and changes in other interacting influences such as climate and land use.
ES.5.2 Nitrogen Enrichment/Eutrophication of Terrestrial, Wetland, and
Aquatic Ecosystems
Terrestrial, wetland, freshwater, and estuarine ecosystems in the U.S. are affected by N
enrichment/eutrophication caused by N deposition. N enrichment/eutrophication refers to
N nutrient-driven changes in growth, physiology, and biodiversity. These effects have
been consistently documented across the U.S. for hundreds of species. New evidence
strengthens the causal relationships for ecosystem N enrichment/eutrophication
determined in the 2008 ISA (Table IS-1).
The 2008 ISA documented that the N enrichment effect in sensitive terrestrial and
wetland ecosystems starts with the accumulation of N in the soil. This increases the
availability of N, a nutrient that increases the growth of some species of soil microbes
and vascular plants at the expense of other species, which may decrease biodiversity.
Since the 2008 ISA, the largest increase in ecological evidence is for terrestrial N driven
enrichment/eutrophication effects (Section IS.5.1, Section IS.5.2; Appendix 4, and
Appendix 6).
This new research confirms the causal relationship between N deposition and ecological
effects documented in the 2008 ISA and improves our understanding of the mechanistic
links that inform causal determinations between N deposition, biogeochemistry, and biota
in terrestrial ecosystems (Table IS-1). A new causal determination has been added to
reflect more specific categories of effects to include physiology, growth, and ecosystem
productivity. Further, there is now stronger empirical evidence from across most regions
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of the U.S. to quantify critical loads (CLs) for N deposition. The figure below provides
estimates of CLs across broad ecoregions and shows the ranges for different functional
groups within these systems (Figure ES-4). Under the CLs, significant harmful effects
from N deposition do not occur according to present knowledge, while at or above CLs,
N deposition can cause a myriad of ecological effects, including decreased tree growth
and increased mortality, and declines in grasses/forbs, lichens, and mycorrhizal fungi.
Since the 2008 ISA, studies have strengthened evidence of species-specific effects of N
deposition on tree growth and mortality in the U.S. Although overall tree growth has
generally been enhanced by N deposition over the last several decades, there is wide
variation among species in growth and mortality responses. Moreover, within some
individual species, N deposition can increase growth and/or survival at low levels, while
decrease growth and/or survival at higher levels. Species with varying responses have
also been shown to co-occur in places in the U.S., suggesting overstory tree community
composition shifts with N deposition.
Since the 2008 ISA, studies have also strengthened the findings of N effects on
decreasing lichen and mycorrhizal fungi biodiversity and provided additional CL
estimates. In terrestrial ecosystems, new evidence provides support that epiphytic lichens
(an algal- and/or cyanobacteria-fungal symbiont) and mycorrhizae (a plant-fungal
symbiosis at the tips of plant roots) are the organisms most sensitive to atmospheric N
deposition and acidifying deposition. Although lichens typically are only a small portion
of terrestrial biomass, these changes in lichen communities are meaningful because
lichens provide food and habitat for insects, birds, and mammals; contribute to nutrient
and hydrologic cycling; have many traditional human uses; and have considerable
potential for pharmaceutical use. Changes in the community composition of mycorrhizal
fungi and declines in mycorrhizal abundance have been observed in the U.S. These fungi
are important for supplying nutrients and water to plants, influencing soil C sequestration,
and producing fruiting bodies (mushrooms) used by humans and wildlife.
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| FASTERN TEMPERATE FORESTS
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¦ MEDITERRANEAN CALIFORNIA
| NORTH AMERICAN DESERTS
| NORTHERN FORESTS
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I I SOUTHERN SEMI-ARID HIGHLANDS
| TEMPERATE SIERRAS
I TROPICAL WET FORESTS
CL = critical load; ha = hectare; kg = kilogram; N = nitrogen; yr = year.
The rectangles indicate the range of CLs designated by Pardo et al. (2011); the circles indicate new papers that have specified CLs;
data from Table 6-28.
Figure ES-4 Summary of critical loads for nitrogen in the U.S. for shrubs and
herbaceous plants (yellow), trees (blue), lichens (green), and
mycorrhizae (gray). Values expressed by major U.S. ecoregions.
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For wetland ecosystems, the 2008 ISA documented that wetlands receiving a larger
fraction of their total water budget in the form of precipitation are more sensitive to the
effects of N deposition. For example, bogs and fens (55-100% of hydro logical input
from rainfall) are more sensitive to N deposition than coastal wetlands (10-20% as
rainfall). Since the 2008 ISA, CLs for U.S. coastal and freshwater wetlands have been
established. The CL for freshwater wetlands is based on C cycling, as well as biodiversity
represented by the morphology and population dynamics of the purple pitcher plant
(Sarraceniapurpurea). The CL for coastal wetlands is based on several different
ecological endpoints, including plant community composition, microbial activity, and
biogeochemistry.
The 2008 ISA documented that the process ofN eutrophication is similar in freshwater
and estuarine ecosystems and typically begins with a nutrient-stimulated algal bloom that
is followed by anoxic conditions. The lack of oxygen in the water due to the respiration
and decomposition of the algae affects higher tropic species. The contribution of N
deposition to total N loading varies among freshwater lakes and stream ecosystems.
Atmospheric deposition is the main source of new N inputs to most headwater stream,
high-elevation lake, and low-order stream watersheds far from the influence of other N
sources like agricultural runoff and wastewater effluent. N deposition was known at the
time of the 2008 ISA to alter biogeochemical processes, nutrient ratios, and
concentrations in recipient freshwater ecosystems. New CLs published since the 2008
ISA support previous observations of increased productivity of phytoplankton and algae,
species changes, and reductions in diversity in atmospherically N enriched lakes and
streams. The productivity of many freshwater ecosystems is N limited. Thus, even small
amounts of N can shift nutrient ratios and affect the trophic status of lakes and streams.
As reported in the 2008 ISA and newer studies, a shift from N limitation to either
colimitation by N and P or limitation by P has been observed in some alpine lakes in the
U.S. and other countries, with these shifts correlated with elevated N deposition.
Estuaries support a large biodiversity of flora and fauna and play a role in nutrient
cycling. At the time of the 2008 ISA, N was recognized as the major cause of harm to the
majority of estuaries in the U.S. Elevated N inputs to coastal areas can alter key processes
that influence N and C cycling in near-coastal environments. Data evaluating sources of
N to estuaries, from the 2008 ISA and newer studies reviewed in this ISA, indicate that N
from atmospheric sources ranges from <10% to approximately 70% of total estuary N
inputs; the atmospheric input for most estuaries is between 15 to 40% of total N inputs. N
from atmospheric and other sources contributes to increased primary productivity,
leading to eutrophication. In some coastal areas eutrophication from N loading may affect
carbonate chemistry under certain circumstances, potentially contributing to acidifying
conditions along with atmospheric anthropogenic CO2 inputs and other factors. Since
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2008, new paleontological studies, observational studies, and experiments have further
characterized the effects of N on phytoplankton growth and community dynamics,
macroinvertebrate response, and other indices of biodiversity in streams, rivers, lakes and
estuaries. For this ISA, new information is consistent with the 2008 ISA, and the causal
determinations for N enrichment in aquatic systems have been updated to reflect more
specific categories of effects, including measures of productivity and altered growth of
biota (Table ES-1).
ES.5.3 Sulfur (S) Enrichment of Wetland and Freshwater Ecosystems
SOx deposition increases SO42 concentration in surface waters. New evidence supports
links between aqueous S concentrations in freshwater ecosystems and both mercury (Hg)
methylation and sulfide toxicity (Table ES-1): however, quantitatively linking these
outcomes to atmospheric deposition remains a challenge.
Increasing SO42 concentration in surface waters can stimulate the microbial
transformation of inorganic Hg into methylmercury (MeHg; Appendix 12). MeHg is the
most persistent and toxic form of Hg affecting animals in the natural environment.
Indicators of S deposition effects upon Hg methylation include increases in MeHg
concentrations or fraction of total Hg in water, sediments, and peat, as well as increases
in MeHg concentrations in periphyton, submerged aquatic plants, invertebrates, and fish.
New evidence confirms the relationship between aqueous concentrations of SO42 and
MeHg and broadens our understanding of where methylation occurs from the wetlands
and lakes reported in the 2008 ISA to include rivers, reservoirs, streams, and saturated
forest soils. Hg methylation occurs at anoxic-oxic boundaries in peat moss and
periphyton, as well as in wetland, lake, estuarine, and marine sediments. There are
published quantitative relationships between surface water SO42 concentrations and
MeHg concentrations, MeHg and total Hg in water, and Hg load in larval mosquitoes and
fish. There is also evidence that decreasing S deposition loads over time (observational
studies of SOx deposition, experimental studies of simulated SOx wet deposition) result
in lower concentrations of MeHg in water, invertebrates, and fish.
There is new evidence since the 2008 ISA to infer a causal relationship between S
deposition and sulfide phytotoxicity, which alters growth and productivity, species
physiology, species richness, community composition, and biodiversity in wetland and
freshwater ecosystems (Appendix 12). This new causal statement reflects new research
on sulfide phytotoxicity in North American wetlands, as the 2008 ISA described sulfide
phytotoxicity only in European ecosystems. Current levels of S deposition cause sulfide
toxicity in wetland and aquatic plants. Indicators of sulfide phytotoxicity caused by S
deposition include increases in water or sediment sulfide concentrations. Sulfide
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negatively effects growth, competitive ability, and persistence in several wetland species,
including the economically important species of wild rice and the keystone sawgrass
species in the Everglades marshes. To date, no published studies have established
regional sensitivities to sulfide phytotoxicity, although studies have observed its effects in
New York, Minnesota, and Florida freshwater marshes. There are no S deposition-based
critical loads for Hg methylation or sulfide phytotoxicity, although researchers have
proposed water quality values to protect biota against these effects in several ecosystems
(Appendix 12).
ES.5.4 Ecological Effects of Particulate Matter Other Than Those Associated
with Nitrogen and Sulfur Deposition
There is a likely causal relationship between PM and ecological effects on biota other
than those associated with N and S deposition (Table ES-1; Appendix 15). Since
publication of the 2009 PM ISA, new literature has built upon the existing knowledge of
ecological effects associated with PM components, especially metals and organics. In
some instances, new techniques have enabled further characterization of the mechanisms
of PM on soil processes, vegetation, and effects on fauna. New studies provide additional
evidence for community-level responses to PM deposition, especially in soil microbial
communities. However, uncertainties remain due to the difficulty in quantifying
relationships between ambient concentrations of PM and ecosystem response.
ES.6 Ecosystem Services
"Ecosystem services" refers to the concept that ecosystems provide benefits to people,
directly or indirectly (Costanza et al.. 2017) and produce socially valuable goods and
services deserving of protection, restoration, and enhancement.
The ecosystem services literature has expanded since the 2008 ISA to include studies that
better characterize ecosystem service valuation and quantification related to acidification
and N enrichment/eutrophication.
Several new studies have paired biogeochemical modeling and benefit transfer equations
informed by willingness-to-pay surveys to estimate the monetary damage done to
ecosystems and the services they provide in the Adirondacks and Shenandoah regions
due to ecosystem acidification (Appendix 14). Despite this progress, for many regions
and specific services, poorly quantified relationships between deposition, ecological
effects, and services are the greatest challenge in developing specific data on the
economic benefits of emission reductions.
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In the 2008 ISA, there were no publications that had specifically evaluated the effects of
N deposition on ecosystem services associated with N driven enrichment/eutrophication.
Since the 2008 ISA, several comprehensive studies have been published on the
ecosystem services related to excessive N in U.S. water bodies. These include an
evaluation of services affected by multiple N inputs (including N deposition) to the
Chesapeake Bay, a synthesis of the cost-benefits on N loading across the nation, an
estimation of the social cost of nitrogen when applied as fertilizer, and an analysis of how
N lost from its intended area of application (e.g., agricultural fields) affects ecosystem
services of adjacent ecosystems. Most notably, new work identifies over 1,000 links
between N deposition and human beneficiaries.
Considering the full body of literature on ecosystem services related to N and S, the
following conclusions are offered: (1) there is evidence thatN and S emissions/deposition
have a range of effects on U.S. ecosystem services and their social value; (2) some
economic studies demonstrate such effects in broad terms, but it remains
methodologically difficult to derive economic costs and benefits associated with specific
regulatory decisions/standards; and (3) numerous, but still inadequately quantified,
relationships are now documented between N and S air pollution and changes in final
ecosystem goods and services.
ES.7 Integrating across Ecosystems
Overall, new evidence since the 2008 ISA increases the weight of evidence for ecological
effects, confirming concepts previously identified and improving quantification of
dose-response (or deposition-ecological indicator) relationships, particularly for N and S
deposition. The ecological effects are described by the causality determinations in
Figure ES-5. which reorganizes the information in Figure ES-3 to show a visualization of
the effects of NOy, SOx, and PM by ecosystem type (e.g., terrestrial, wetland, freshwater,
and estuarine). With this organization, the multiple effects occurring in each ecosystem
due to various pollution combinations of NOy, SOx, and PM are emphasized. Between
two and four different classes of pollutant effects may occur in each ecosystem type in
the U.S. For more information on key messages, see the expanded discussion in the
Integrated Synthesis; detailed information on specific ecosystem types and specific
classes of pollutant effects included in the ISA may be found in the appendices.
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Estuary-
Ecosystem
Causality framework
Inadequate
Not evaluated in causal framework
Causal
Likely causal
* Includes: NO. N02. HN03, S02, and PAN
Figure ES-5 Causal relationships between the criteria pollutants and ecological effects organized under
ecosystem type.
N-enrichment/
Eutrophjcaton
H-enrichment/
Eutroptwcatkxn
ff-enrchmervt/
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M-enrichrrveniV
Eutrophcatbn
Mercury
Methyiatjon
Mercury
Methyiation
Class of Poiutarvt Effect
Ackfifscafton
Sulfide Ittratity
N'+5 dep
N+S
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ES.8 References
Costanza. R; De Groot R: Braat L; Kubiszewski. I; Fioramonti. L; Sutton. P; Farber. S;
Grasso, M. (2017). Twenty years of ecosystem services: How far have we come and how
far do we still need to go? Ecosyst Serv 28: 1-16.
http://dx.doi.Org/10.1016/i.ecoser.2017.09.008
Pardo, LH; Fenn, ME: Goodale, CL; Geiser, LH; Driscoll, CT; Allen. EB; Baron. JS:
Bobbink. R; Bowman. WD: Clark. CM: Emmett. B; Gilliam. FS: Greaver. TL; Hall. SJ:
Lilleskov, EA: Liu, L: Lynch, JA: Nadelhoffer, KJ: Perakis, SS: Robin-Abbott, MJ:
Stoddard, JL: Weathers, KC: Dennis, RL. (2011). Effects of nitrogen deposition and
empirical nitrogen critical loads for ecoregions of the United States. Ecol Appl 21: 3049-
3082. http://dx.doi.Org/10.1890/10-2341.l
U.S. EPA (U.S. Environmental Protection Agency). (2008). Integrated science assessment for
oxides of nitrogen and sulfur: Ecological criteria [EPA Report], (EPA/600/R-08/082F).
Research Triangle Park, NC: U.S. Environmental Protection Agency, Office of Research
and Development, National Center for Environmental Assessment- RTP Division.
http://cfpub.epa. gov/ncea/cfm/recordisplav.cfm?deid=201485
U.S. EPA (U.S. Environmental Protection Agency). (2009). Integrated science assessment for
particulate matter [EPA Report], (EPA/600/R-08/139F). Research Triangle Park, NC: U.S.
Environmental Protection Agency, Office of Research and Development, National Center
for Environmental Assessment- RTP Division.
http://cfpub.epa. gov/ncea/cfm/recordisplav.cfm?deid=216546
U.S. EPA (U.S. Environmental Protection Agency). (2011). Policy assessment for the review
of the secondary national ambient air quality standards for oxides of nitrogen and oxides of
sulfur [EPA Report], (EPA-452/R-1 l-004a). Washington, DC.
http://www3.epa.gov/ttn/naaqs/standards/no2so2sec/data/2011Q114pamain.pdf
U.S. EPA (U.S. Environmental Protection Agency). (2015). Preamble to the integrated
science assessments [EPA Report], (EPA/600/R-15/067). Research Triangle Park, NC:
U.S. Environmental Protection Agency, Office of Research and Development, National
Center for Environmental Assessment, RTP Division.
https://cfpub.epa.gOv/ncea/i sa/recordisplay.cfm?deid=310244
U.S. EPA (U.S. Environmental Protection Agency). (2016a). Integrated science assessment
(ISA) for sulfur oxides health criteria (Second external review draft) [EPA Report],
(EPA/600/R-16/351). Washington, DC.
https://cfpub.epa.gOv/ncea/i sa/recordisplay.cfm?deid=326450
U.S. EPA (U.S. Environmental Protection Agency). (2016b). Integrated science assessment
for oxides of nitrogen-health criteria (final report) [EPA Report], (EPA/600/R-15/068).
Research Triangle Park, NC: U.S. Environmental Protection Agency, Office of Research
and Development, National Center for Environmental Assessment.
http://ofmpub.epa.gov/eims/eimscomm.getfile7p download id=526855
U.S. EPA (U.S. Environmental Protection Agency). (2019). U.S. EPA Integrated Science
Assessment for particulate matter [EPA Report], (EPA/600/R-19/188).
https://cfpub.epa.gOv/ncea/i sa/recordisplay.cfm?deid=347534
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