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## Ozone-Induced Symptoms on Vegetation within the Moosehorn National Wildlife Refuge in Maine

Author(s): Donald D. Davis Source: Northeastern Naturalist, 14(3):403-414. 2007. Published By: Eagle Hill Institute

DOI: http:// dx.doi.org/10.1656/1092-6194(2007)14[403:OSOVWT]2.0.CO;2

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### Ozone-Induced Symptoms on Vegetation within the Moosehorn National Wildlife Refuge in Maine

Donald D. Davis 1

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), Populusspp. (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 andClass-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 ofPrevention 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 “MoosehornWilderness”. In 1978, the Moosehorn Wilderness was designated a ClassI 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

1 Department of Plant Pathology, Ecology Faculty, and Penn State Institutes of theEnvironment, 211 Buckhout Laboratory, The Pennsylvania State University, University Park, PA 16802; ddd2@psu.edu.Northeastern Naturalist Vol. 14, No. 3 404 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), Carexspp. (sedges), and Cornus canadensis L. (bunchberry). Wetlands include beaverponds 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

minorGmelin (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 bioindicatorplants 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).D.D. Davis 2007 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 throughoutmuch 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 betweenozone injury and ozone levels or soil-moisture stress. To meet these objectives, surveys were conducted during 1998–2000 and 2002–2004.Northeastern Naturalist Vol. 14, No. 3 406

Methods

Prior to the initial 1998 survey, the author examined maps of theMoosehorn 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).D.D. Davis 2007 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%Northeastern Naturalist Vol. 14, No. 3 408 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 commonfoliar 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 meanD.D. Davis 2007 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. 18,000ppb-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 morepristine 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).Northeastern Naturalist Vol. 14, No. 3 410 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.D.D. Davis 2007 411
analysis (Minitab 2003) revealed that logistic models could not be used to predict the relationships, largely due to the limited number of years ofobservations. 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 correlationanalysis (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 generallyrespond 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).Northeastern Naturalist Vol. 14, No. 3 412 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 anddirect, 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 factorsthat 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 speciesD.D. Davis 2007 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.Northeastern Naturalist Vol. 14, No. 3 414
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 (O
3 ) 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/P93/004Af. 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 toevaluate ambient ozone concentrations in north central Pennsylvania. Environmental Pollution 125:71–80. Zierl, B. 2001. A water-balance model to simulate drought in forested ecosystemsand its application to the entire forested area in Switzerland. Journal of Hydrology 242:115–136.