Access Journal Content
Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.
Current Issue: Vol. 30 (3)
Check out NENA's latest Monograph:
Monograph 22
2007 NORTHEASTERN NATURALIST 14(3):403–414
Ozone-Induced Symptoms on Vegetation within the
Moosehorn National Wildlife Refuge in Maine
Donald D. Davis1
Abstract - During 1998–2000 and 2002–2004, field surveys were conducted within
the Moosehorn National Wildlife Refuge, located in northeastern Maine, to determine
if ozone-induced symptoms occurred on refuge vegetation. Foliar symptoms were
observed on ozone-sensitive bioindicators during each survey year, but the incidence
(percentage) of plants exhibiting symptoms was generally low and varied among
species and years. Refuge plants that exhibited symptoms included Fraxinus spp.
(ash), Populus spp. (aspen), Corylus cornuta (beaked hazelnut), Prunus serotina
(black cherry), Prunus pensylvanica (pin cherry), Apocynum androsaemifolium
(spreading dogbane), and a viburnum tentatively identified as Viburnum nudum var.
cassinoides (withe-rod). Data from the nearest US EPA ozone-monitoring site, located
113 km southwest of the refuge in Acadia National Park, ME, revealed that ambient
SUM60 ozone levels during survey years ranged from approximately 17,900 ppb-hrs
in 2000 to more than 40,000 ppb-hrs in 1998. Therefore, the threshold level of SUM60
ozone capable of inducing symptoms on sensitive vegetation within this refuge and
Class-I Wilderness area is less than 18,000 ppb-hrs, and may be as low as 10,000 ppbhrs.
The results of these surveys can be used by the US Fish and Wildlife Service when
making air-quality management decisions, including those related to the review of
Prevention of Significant Deterioration permits, and might serve as input into formulating
more stringent National Ambient Air Quality Standards for ozone.
Introduction
The Moosehorn National Wildlife Refuge (NWR), located in northeastern
Maine near the US–Canadian border, was established in 1937 as a
refuge and breeding ground for migratory birds and wildlife. The refuge
consists of two divisions: the 6507-ha Baring Division, located southwest
of Calais, and the 2697-ha Edmunds Division, adjacent to the ocean at
Cobscook Bay near Dennysville (Fig. 1). In 1975, approximately 1894 ha
of the Baring Division and 1125 ha of the Edmunds Division were
deemed wilderness areas by the US Congress and named the “Moosehorn
Wilderness”. In 1978, the Moosehorn Wilderness was designated a Class-
I air-quality area, receiving further protection under the Clean Air Act as
amended in 1977 (US Congress 1977). At that time, the US Congress
gave the US Fish and Wildlife Service (USFWS), as well as other federal
land managers of Class-I areas, an affirmative responsibility to protect all
air-quality related values (AQRVs) in Class-I areas (US Congress 1977).
AQRVs include vegetation, wildlife, water, soils, visibility, and cultural
1Department of Plant Pathology, Ecology Faculty, and Penn State Institutes of the
Environment, 211 Buckhout Laboratory, The Pennsylvania State University, University
Park, PA 16802; ddd2@psu.edu.
404 Northeastern Naturalist Vol. 14, No. 3
resources. By federal law, AQRVs in Class-I areas must be protected
from deterioration. However, despite this special protection, significant
levels of ambient ozone still impinge on many Class-I air-quality areas in
the Northeast, adversely affecting AQRVs (Lefohn and Manning 1995,
Manning et al. 1996).
Refuge vegetation
Hardwood trees in the Moosehorn NWR include Populus tremuloides
Michx. (quaking apen), P. grandidentata Michx. (bigtooth aspen), Betula
papyrifera Marsh. (paper birch), B. populifolia Marsh. (gray birch), Acer
rubrum L. (red maple), Fagus grandifolia Ehrh. (American beech), Prunus
serotina Ehrh. (black cherry), and Prunus pensylvanica L. (pin cherry).
Coniferous trees include Abies balsamea L. (balsam fir), scattered Pinus
strobus L. (eastern white pine), and various Picea spp. (spruces). Pure
stands of Alnus rugosa (Du Roi) Spreng. (alder) occur within abandoned
farmlands, as well as along the edges of streams and beaver flowages.
Common understory plant species include Gaultheria procumbens L. (wintergreen),
Pteridium aquilinum (L.) Kuhn (bracken fern), Carex spp.
(sedges), and Cornus canadensis L. (bunchberry). Wetlands include beaver
ponds and beaver meadows; marsh, shrub, and forested wet areas of various
types; and natural ponds, streams, and lakes. Several Vaccinium spp.
(blueberry) fields are maintained as permanent forest openings. A longterm
forest management plan, including cutting and burning of small
blocks of forest vegetation within the refuge, has been utilized since 1976
to increase the diversity of forest habitat, primarily to favor Scolopax
minor Gmelin (American woodcock). In the Cobscook Bay area, there are
open hayfields, as well as abandoned farms in various stages of succession.
Since the discovery that leaf “stipple” of Vitis spp. (grapes) was caused
by ozone (Richards et al. 1958), this characteristic symptom has been used to
evaluate ozone injury on broadleaved bioindicator plants. Stipples usually
appear as 1–2-mm diameter areas of pigmented, black or reddish-purple
tissue, restricted by the veinlets, on the adaxial surface of mature leaves (for
illustrations, see Skelly 2000). Immature leaves seldom exhibit stipple, and
premature defoliation of injured leaves may occur on sensitive species. To
the casual observer, these symptoms are similar to those induced by other
stresses (i.e., nutrient deficiency, early fall coloration, and heat stress).
However, the pigmented, adaxial stipple on sensitive plants is a reliable
diagnostic symptom that can be used by experienced observers to evaluate
and quantify ozone injury during field surveys (Skelly 2000).
Prior to the initial survey, the author examined unpublished refuge
flora lists and noted the presence of several bioindicator plants known to
be sensitive to ozone. The ozone-sensitivity of these potential bioindicator
plants has since been summarized (US DOI 2003). Potential bioindicator
plants growing in the Moosehorn NWR included Sambucus canadensis
L. (American elder), bigtooth aspen, black cherry, pin cherry, Viburnum
spp. (viburnums), and Fraxius americana L. (white ash).
2007 D.D. Davis 405
Ambient ozone levels
Ground-level ozone is the most important plant-damaging air pollutant in
the US and Canada, and elevated levels of ozone occur annually throughout
much of eastern North America (Comrie 1994, Coulston et al. 2003). Elevated
ozone concentrations are capable of injuring native plants in many
rural locations, including wilderness areas (Lefohn and Manning 1995,
Manning et al. 1996) and wildlife refuges (Davis and Orendovici 2006).
During these field studies, the EPA ozone monitor (AIRS site #23-009-
0102) nearest to the Moosehorn NWR was located within Acadia National
Park (NP), ME, approximately 113 km southwest (generally upwind) of the
refuge. Monitoring data have revealed that Acadia NP experiences some of
the highest concentrations of ozone on the east coast (Kohut et al. 2000). The
ozone, or its precursors, that affects the coast of Maine likely originates in
the megalopolis along the eastern seaboard to the southwest and upwind
from the refuge (Cleveland et al. 1976, Kohut et al. 2000). This ozone, or its
precursors, can travel downwind for hundreds of km during long-range
transport, as influenced by wind direction and weather fronts, and impinge
upon vegetation at the Moosehorn NWR.
Prior to the initial survey, the author examined the 1996 and 1997
ozone-monitoring data collected at Acadia NP and concluded that ambient
ozone had occurred at phytotoxic concentrations within this national park.
Assuming that these ozone levels also occurred in the Moosehorn NWR, and
the fact that ozone-sensitive plant species were listed as growing in the
refuge, the author hypothesized that ambient ozone was likely to injure
sensitive plants within the refuge.
Phytotoxic levels of ozone in the northeastern US would likely occur during
the vegetative growing season, from spring to fall. Therefore, the daily ozone
data from April 1 to September 31 during the survey years of 1998–2000 and
2002–2004 were examined. In this paper, ozone levels are expressed as
SUM60, the accumulation of ozone concentrations of 60 ppb or greater during
the growing season. The SUM60 ozone metric was of interest since it had been
correlated with ozone-induced symptoms on forest trees in the eastern US
(Hildebrand et al. 1996). However, the impact of ambient ozone levels can be
confounded by soil-moisture stress. Soil-moisture stress can induce stomatal
closure, limiting gas exchange and ozone uptake by vegetation, thereby
reducing or eliminating subsequent ozone injury (Showman 1991, Yuska et al.
2003). Soil-moisture stress may be the most important environmental factor
controlling the response of plant stomata during the growing season (Zierl
2001). Therefore, soil-moisture stress during survey years was evaluated using
the Palmer Drought Severity Index (PDSI; Palmer 1965).
The objectives of this study were to determine: 1) if ozone injury occurred
on plants within the Moosehorn NWR, 2) the incidence (percentage)
of bioindicator plants exhibiting stipple, and 3) the relationship between
ozone injury and ozone levels or soil-moisture stress. To meet these objectives,
surveys were conducted during 1998–2000 and 2002–2004.
406 Northeastern Naturalist Vol. 14, No. 3
Methods
Prior to the initial 1998 survey, the author examined maps of the
Moosehorn NWR to select tentative survey sites. Tentative sites were chosen
within open areas, along roadsides, and the edge of fields, where
bioindicators were exposed to unrestricted air movement and direct sunlight,
criteria required for suitable sampling sites (Anderson et al. 1989). Twentyfive
potential survey sites were visited in 1998, and 15 survey sites were
selected from these based on openness, accessibility, and presence of
bioindicators. During 1999 and succeeding survey years, some of these 15
sites were relocated slightly, othes eliminated, and new sites added as
species composition changed due to natural succession. However, the
Figure 1. Map showing location of 15 survey sites (open double circles) within the
two divisions (Baring and Edmunds) of the Moosehorn National Wildlife Refuge in
northeastern Maine. (Map courtesy of the US Fish and Wildlife Service).
2007 D.D. Davis 407
general location of these 15 sites formed the basis for the field survey. Eight
sites in the Baring Division and seven in the Edmonds Division were used
during most survey years (Fig. 1). Data were not taken at each site each year,
depending mainly on degres of insect injury to the foliage of the bioindicator
plants at the site. Plants with servere foliar injury from insects were not
rated. The primary bioindicator plants examined during the survey are listed
in Table 1.
The refuge was surveyed twice in 1998: during July 29–August 2 and
August 25–28. In 1999 and succeeding survey years, the refuge was visited
only once. In 1999, the refuge was surveyed during July 22–25, and it was
surveyed in 2000 from August 21–23. The refuge was not surveyed in 2001.
In 2002, surveys were conducted during the periods August 29–September
2, August 6–8 in 2003, and August 20–22 in 2004.
During each survey year, the number of plants that exhibited classic
ozone-induced stipple was recorded. Mainly saplings of the woody
Table 1. Summary of observations made during the 1998–2000 and 2002–2004 surveys at the
Moosehorn National Wildlife Refuge (the refuge was not surveyed in 2001). Numbers in table
refer to number of plants with ozone-induced stipple as compared to the total number of plants
evaluated for that species-genus; data also expressed as percentages.
Black Pin Spreading
Year (survey date) Ash Aspen cherry cherry dogbane Viburnum
1998 (July 29–Aug 2)
Number plants examined 54 143 55 109 106
Number plants injured 1 12 0 24 12
Percentage 1.8% 8.4% 0.0% 22.0% 11.3%
1998 (Aug 25–28)
Number plants examined 81 86 51 108
Number plants injured 2 2 5 28
Percentage 2.5% 2.3% 9.8% 25.9%
1999 (July 22–25)
Number plants examined 77 396 111 196 178
Number plants injured 2 9 5 4 10
Percentage 2.6% 2.3% 4.5% 2.0% 5.6%
2000 (Aug 21–23)
Number plants examined 150 154 86 176 120 10
Number plants injured 6 12 0 13 24 2
Percentage 4.0% 7.8% 0.0% 7.4% 20.0% 20.0%
2002 (Aug 29–Sept 1)
Number plants examined 117 559 60 243 344 12
Number plants injured 4 39 0 6 45 2
Percentage 3.4% 5.4% 0.0% 2.5% 13.1% 16.7%
2003 (Aug 6–8)
Number plants examined 163 166 43 282 307 46
Number plants injured 1 1 0 2 2 6
Percentage 0.6% 0.6% 0.0% 0.7% 0.6% 13.0%
2004 (Aug 20–22)
Number plants examined 153 265 65 315 30 30
Number plants injured 6 0 0 0 0 0
Percentage 4.5% 0.0% 0.0% 0.0% 0.0% 0.0%
Average 2.8% 4.2% 2.1% 5.4% 8.6% 10.2%
408 Northeastern Naturalist Vol. 14, No. 3
bioindicators (ash, aspens, cherries, viburnum) were evaluated; some aspen
seedlings were rated. No attempt was made to evaluate mature, canopy trees.
Stipple was noted as present or absent for individual plants. Incidence was
calculated as (number of symptomatic plants)/(number of plants examined for
each species-genus) and expressed as a percentage. Factors that can influence
ozone injury incidence include plant-species sensitivity (US DOI 2003),
SUM60 ozone level (Hildebrand et al. 1996), and drought stress (Showman
1991, Yuska et al. 2003). We previously used binomial logistic regression to
successfully disclose the presence and strength of significant relationships
between incidence (presence or absence) of ozone induced-symptoms and
these factors in a similar, but larger, study within a NWR in New Jersey (Davis
and Orendovici 2006). Therefore, a binomial logistic regression analysis was
used herein to investigate significant relationships between incidence of
ozone injury and the following factors: plant species, ozone level, and drought
stress. Severity (as opposed to incidence) of injury was not evaluated. To
illustrate the ambient ozone levels that likely impinge upon the refuge, the
SUM60 ozone levels from Acadia NP were examined and graphed for each
survey year.
Results and Discussion
Symptom description and incidence
The classic dark, adaxial, ozone-induced stipple was the most common
foliar symptom observed on bioindicators within the Moosehorn NWR. During
the first year of the survey (1998), the author observed that Apocynum
androsaemifolium L. (spreading dogbane) and a viburnum tentatively identified
as Viburnum nudum L. var. cassinoides (L.) Torr. & Gray (withe-rod)
also exhibited adaxial stipple typical of that caused by ozone. Therefore,
spreading dogbane and withe-rod were added to the list of potential
bioindicators. In addition, stippling was also noted on Corylus cornuta Marsh.
(beaked hazelnut) shrubs in 2002 and 2003 (data not shown). However, the
stipple on hazelnut was very slight and difficult to evaluate in a consistent
manner; it was noted but not recorded as data.
Ash, aspen, cherry, and dogbane were the most common bioindicators in
the refuge. Based on the appearance of emerging seedlings, it was difficult to
distinguish between the two ash species, as well as the two aspen species.
Therefore, these plants were identified only as ash and aspen. Red foliage,
chlorotic stipple, and premature defoliation symptoms were noted occasionally
on bioindicators, but these were not recorded as data. Although such
symptoms have been induced by ozone under controlled conditions, they also
may be caused by other factors such as high temperature, low soil moisture,
and early autumnal coloration (Orendovici et al. 2003).
Bioindicators within the refuge exhibited ozone-induced symptoms during
most survey years (Table 1). However, the data most comparable for
statistical analyses were from the August surveys of 1998, 2000, 2002, and
2004. The ozone-sensitivity ranking of the bioindicators, based on mean
2007 D.D. Davis 409
percentage of individuals exhibiting stipple across these 4 most-comparable
years, was spreading dogbane (14.0%) > viburnum (7.7%) > pin cherry
(5.6%) > aspen (5.0%) > ash (3.6%) > black cherry (1.9%). Spreading
dogbane was judged to be the most sensitive bioindicator plant in the refuge.
The high sensitivity of spreading dogbane to ambient ozone has been confirmed
in both open-top chamber studies and field surveys (Bergweiler and
Manning 1999, Eckert et al. 1999, Kohut et al. 2000). However, leaves of
spreading dogbane often became highly chlorotic and spotted, and began to
senesce by late summer, making it an unsuitable bioindicator later in the
growing season. Spreading dogbane would be more useful as an ozone
bioindicator in Maine early in the growing season, before the onset of
confounding symptoms that could mask ozone-induced stipple.
Viburnums, pin cherry, and aspen were the next most useful bioindicators,
all of which have been reported to be sensitive to ozone (US DOI 2003).
Although black cherry is considered to be very sensitive to ozone (Davis and
Skelly 1992, Davis et al. 1981), this species exhibited the lowest incidence
(1.9%) of any bioindicators. This low level of ozone injury was similar to the
incidence of ozone injury on black cherry during similar surveys within a NWR
in New Jersey, conducted within the same time frame (Davis and Orendovici
2006). For unknown reasons, black cherry might not be a useful bioindicator
for evaluating ozone injury along the coast of northeastern US. It is possible
that ozone-sensitive genotypes have been eliminated from the population.
Ambient ozone levels
During the survey years (1998–2000, 2002–2004), the August SUM60
ozone levels monitored at the EPA monitor in Acadia National Park were
highest in 1998 (ca. 40,000 ppb-hrs) and lowest in 2000 and 2004 (ca. 18,000
ppb-hrs) (Fig. 2). By late August, SUM60 ozone levels in 2002 were approximately
33,000 ppb-hrs, 29,000 ppb-hrs in 1999, and 26,000 ppb-hrs in 2003.
The overall pattern of ozone accumulation during the growing season was
similar from year to year, showing a gradual increase from May to September,
and a slight decrease thereafter. An exception to this trend occurred in 2002,
when the ambient ozone increased rapidly in early August.
In contrast to other wildlife refuges in eastern US, ozone levels monitored
in Acadia NP were slightly greater than those monitored within the more
pristine Seney NWR located in the remote upper peninsula of northern Michigan.
SUM60 ozone monitored within the Seney refuge (EPA AIRS Site #26-
153-0001) was usually quite low, in the range of 5000–15,000 ppb-hrs by the
end of the growing season. In contrast to the relatively pristine Moosehorn and
Seney refuges, SUM60 ozone levels within the Forsythe NWR (EPA AIRS site
#34-001-0005) in New Jersey often exceeded 40,000 ppb-hrs by the end of the
summer, and has been reported as high as 70,000 ppb-hrs (Davis and
Orendovici 2006). Similarly, high SUM60 ozone levels, exceeding 70,000
ppb-hrs by late summer, have been reported in southeastern Missouri near the
Mingo NWR (as extrapolated from the nearest ozone monitor, EPA AIRS Site
#29-186-0005).
410 Northeastern Naturalist Vol. 14, No. 3
Relationship of incidence to species, ozone, and drought
As stated earlier, the most comparable incidence data were from the
August surveys of 4 years: 1998, 2000, 2002, and 2004. A binomial logistic
regression analysis (Davis and Orendovici 2006) was run on these 4 years’
data to determine if incidence of ozone injury was related to plant species,
ozone level, and drought stress. However, the Pearson goodness-of-fit
Figure 2. Sum of hourly ozone concentrations equaling or exceeding 60 ppb
(SUM60, ppb-hrs) recorded from May 1 to September 31, 1998–2000 (upper) and
2002–2004 (lower), at EPA AIRS Site #23-009-0102, located within the Acadia
National Park, 113 km southwest from the Moosehorn National Wildlife Refuge.
2007 D.D. Davis 411
analysis (Minitab 2003) revealed that logistic models could not be used to
predict the relationships, largely due to the limited number of years of
observations. The regression results (based on chi-square analysis) did reveal
that significant differences (p = 0.05) in ozone incidence occurred
among species, ozone level, and drought stress (but could not be used for
predictive purposes). Therefore, data were analyzed using simple correlation
analysis (Minitab 2003) to evaluate the direction of relationships (not predictions)
between incidence of stipple as compared to plant species/genus,
SUM60 ozone as of date of survey, and PDSI at the end of August (Fig. 3).
The incidence of ozone injury of aspen was significantly correlated with
that of spreading dogbane and viburnum, but not with the other species/
genera. This finding indicates that dogbane and viburnum may generally
respond in similar manner to ozone and/or environmental factors. The incidence
of injury on black cherry was significantly correlated only with that of
pin cherry, indicating that the two Prunus species were responding to ozone or
the environment in a similar manner from year to year.
Figure 3. Palmer Drought Severity Index for coastal Maine, including Moosehorn
NWR, during 1895–2004. The horizontal line at “0” is considered normal moisture
levels. Areas above the line represent more than adequate moisture for normal plant
functioning, whereas areas below the line represent potential water stress. A drought
severity index of -3 is a severe drought, likely closing stomata and reducing ozone
uptake (data from http://www.ncdc.noaa.gov/oa/climate/onlineprod/drought/
xmgr.html).
412 Northeastern Naturalist Vol. 14, No. 3
Incidence of ozone injury for any of the six bioindicator species was not
significantly correlated (p = 0.05) with ambient SUM60 ozone levels. The
relationship between injury and level of ambient ozone is seldom simple and
direct, but is confounded by interacting environmental factors such as soilmoisture
stress (Davis and Orendovici 2006). In fact, Manning (2003) stated
that use of cumulative ozone data as threshold values for predicting ozone
injury to plants must take into account biological and environmental factors
that affect ozone uptake via stomata. Soil-moisture stress can induce stomatal
closure, which limits ozone uptake, thereby reducing or eliminating
subsequent ozone injury (Showman 1991, Yuska et al. 2003). Similarly,
Eckert et al. (1999) reported no relationship between ambient ozone levels in
Acadia NP and ozone injury on park vegetation, and also attributed this lack
of correlation to the confounding effects of moisture stress on stomatal
functioning. Along these lines, the incidence of ozone injury on aspen,
spreading dogbane, and viburnum, but not the other three bioindicators, at
Moosehorn NWR was negatively correlated (p = 0.05) with PDSI drought
stress. However, since the correlation was only significant for three of the
six bioindicators, the relationship between ozone injury and soil-moisture
stress apparently varies with plant species. In addition, the relationship
likely varies with the level of moisture stress. Plants operating at adequate
soil-moisture level, above some critical threshold, are likely to be more
responsive to varying amounts of ambient ozone. Plants operating under
moisture stress would not likely respond to varying ozone levels since
stomatal uptake of ozone would be limited.
The considerable distance between the Moosehorn NWR and the ozone
monitor at Acadia NP may also have obscured any relationship between
ambient ozone levels and incidence of plant injury that occurred within the
refuge. More long-term databases, involving field observations, are needed
to accurately relate ozone-induced injury with ambient levels of ozone.
Nevertheless, if the SUM60 ozone levels measured at Acadia National
Park, 113 km southwest from the Moosehorn NWR, were comparable to
those ozone levels reaching the refuge, then the threshold level for ozone
to induce symptoms on sensitive plants within the Moosehorn refuge was
likely near 10,000 ppb-hrs. This indicates that ozone injury might have
occurred on sensitive plants in the refuge by early June in 1998, and by late
June to early July in the other survey years (Fig. 2). Threshold ozone
concentrations could have exceeded phytotoxic levels as early as late June–
early July. If so, ozone might have injured sensitive species within the
Moosehorn refuge more than a month before most ozone injury surveys,
which are normally conducted in mid- to late-August. Results of the first
survey, conducted during July 29–August 2, 1998, supports this hypothesis,
since considerable ozone injury had already occurred within the Moosehorn
NWR by late July of that high-ozone year.
Given that high ozone levels occurred in 1998, it is possible that ozone
injury occurred in the refuge as early as May of that year. Plant species
2007 D.D. Davis 413
emerging and completing their life cycles early in the growing season, such
as late-spring or early-summer ephemerals, might be at risk in Maine in early
to mid-summer when SUM60 ozone levels exceed 10,000 ppb-hrs (Fig. 2).
Ozone injury on these ephemeral plants would likely go undetected during
August, when most ozone-injury surveys are conducted in the East, and
might represent an undetected threat to natural ecosystems (Davis
and Orendovici 2006). If the threshold value of ozone needed to cause injury
on such species is less than 10,000 ppb-hrs, then injury could occur even
earlier on sensitive plants in the refuge.
The findings of the present study revealed that bioindicators within the
Moosehorn NWR exhibited ozone-induced symptoms during each survey
year (1998–2000, 2002–2004). Eckert et al. (1999) reported that injury from
ambient ozone was observed on sensitive vegetation within the Acadia NP
during 1995–1997. Therefore, if ambient ozone levels at the Moosehorn
NWR are similar to those monitored at Acadia NP, it is likely that the
ambient ozone levels at the Moosehorn NWR are high enough in most years
to cause injury on sensitive refuge plants, including those growing in the
Class-I wilderness area. The US Fish and Wildlife Service can use the results
of these surveys when making air-quality management decisions, including
those related to review of Prevention of Significant Deterioration permits,
and such data can be used to strengthen our National Ambient Air Quality
Standards for ozone (US EPA 1996).
Acknowledgments
The author gratefully acknowledges receiving financial support from the US Fish
and Wildlife Service, Air Quality Branch, Denver, CO, and acknowledges receiving
ozone datasets from Mr. David Joseph, National Park Service, Denver, CO.
Literature Cited
Anderson, R.L., C.M. Huber, R.P. Belanger, J. Knighten, T. McCartney, and B.
Book. 1989. Recommended survey procedures for assessing on bioindicator
plants in Region-8 Class-1 Wilderness areas. USDA Forest Service, Forest Pest
Management, Asheville Field Office, Asheville, NC. Report 89-1-36. 6 pp.
Bergweiler, C.J., and W.J. Manning. 1999. Inhibition of flowering and reproductive
success in spreading dogbane, Apocynum androsaemifolium (L.), by exposure to
ambient ozone. Environmental Pollution 105:333–339.
Cleveland, W.S., J.C. McRae, and J.C. Warner. 1976. Photochemical air pollution:
Transport from the New York City area to Connecticut and Massachusetts.
Science 191:179–181.
Comrie, A.C. 1994. A synoptic climatology of surface ozone in rural ozone pollution
at three forest sites in Pennsylvania. Atmospheric Environment 28:1601–1614.
Coulston, J.W., G.C. Smith, and W.D. Smith. 2003. Regional assessment of ozone
sensitive tree species using bioindicator plants. Environmental Monitoring and
Assessment 83:117–127.
Davis, D.D., and T. Orendovici. 2006. Incidence of ozone symptoms on vegetation
within a National Wildlife Refuge in New Jersey, USA. Environmental Pollution
143:555–564.
414 Northeastern Naturalist Vol. 14, No. 3
Davis, D.D., and J.M. Skelly. 1992. Foliar sensitivity of eight eastern hardwood tree
species to ozone. Water, Air, and Soil Pollution 62:269–277.
Davis, D.D., D.M. Umbach, and J.B. Coppolino. 1981. Susceptibility of tree and
shrub species and response of black cherry foliage to ozone. Plant Disease
65:904–907.
Eckert, R., R. Kohut, T. Lee, and K. Stapelfeldt. 1999. Foliar ozone injury on native
vegetation at Acadia National Park: Results from a six-year (1992–1997) field
survey. National Park Service Boston, MA. Technical Report NPS/BSO-RNR/
NRTR/00-12. 41 pp.
Hildebrand, E., J.M. Skelly, and T.S. Fredericksen. 1996. Foliar response of ozone
sensitive hardwood tree species from 1991 to 1993 in the Shenandoah National
Park, VA. Canadian Journal for Forestry Research 26:658–669.
Kohut, R., J. Laurence, P. King, and R. Raba. 2000. Identification of bioindicator
species for ozone and assessment of the responses to ozone of native vegetation
at Acadia National Park. National Park Service, Boston, MA. Technical Report
NPS/BSO-RNR/NRTR/00-13. 126 pp.
Lefohn, A.S., and W.J. Manning. 1995. Ozone exposures near Class-I wilderness
areas in New Hampshire and Vermont. Atmospheric Environment 29:601–606.
Manning, W.J. 2003. Detecting plant effects is necessary to give biological significance
to ambient-ozone monitoring data and predictive ozone standards. Environmental
Pollution 126:375–379.
Manning, W.J., S.V. Krupa, C.J. Bergweiler, and K.I. Nelson. 1996. Ambient ozone
(O3) in three Class-I wilderness area in northeastern USA: Measurements with
Ogawa passive samplers. Environmental Pollution 91:399–403.
Minitab Inc. 2003. Quality Plaza, 1829 Pine Hall Road, State College, PA, 16801.
Orendovici, T., J.M. Skelly, J.A. Ferdinand, J.E. Savage, M.-J. Sanz, and G.C.
Smith. 2003. Response of native plants of northeastern United States and southern
Spain to ozone exposures: Determining exposure/response relationships.
Environmental Pollution 125:31–40.
Palmer, W.C. 1965. Meteorological drought. Research Paper Number 45. US Department
of Commerce, Washington, DC. 58 pp.
Richards, B.L., J.T. Middleton, and W.B. Hewitt. 1958. Air pollution with relation to
agronomic crops. V. Oxidant stipple of grape. Agronomy Journal 50:559–561.
Showman, R.E. 1991. A comparison of ozone injury to vegetation during moist and
drought years. Journal Air and Waste Management Association 41:63–64.
Skelly, J.M. 2000. Tropospheric ozone and its importance to forests and natural plant
communities of the northeastern United States. Northeastern Naturalist 7:221–236.
United States Congress (US Congress). 1977. The Clean Air Act as amended August
1977. P.L. 95-95. US Government Printing Office, Washington, DC.
United States Department of the Interior (US DOI). 2003. Ozone-sensitive plant
species on National Park Service and US Fish and Wildlife Service Lands:
Results of a June 24–25, 2003 Workshop, Baltimore, MD. US DOI, Denver, CO.
Natural Resource Report NPS/NRARD/NRR-2003/01. 21 pp.
United States Environmental Protection Agency (US EPA). 1996. Air-quality criteria
for ozone and related photochemical oxidants. Vol. 1 of 3 reports. EPA/600/P-
93/004Af. Research Triangle Park, NC.
Yuska, D.E., J.M. Skelly, J.A. Ferdinand, R.E. Stevenson, J.E. Savage, J.D. Mulik,
and A. Hines. 2003. Use of bioindicators and passive sampling devices to
evaluate ambient ozone concentrations in north central Pennsylvania. Environmental
Pollution 125:71–80.
Zierl, B. 2001. A water-balance model to simulate drought in forested ecosystems
and its application to the entire forested area in Switzerland. Journal of Hydrology
242:115–136.